Spectroscopic and electronic structural studies of blue copper model complexes. 2. Comparison of three-and four-coordinate Cu(II)-thiolate complexes and fungal laccase

11632

J. Am. Chem. Soc. 2000, 122, 11632-11648

Spectroscopic and Electronic Structural Studies of Blue Copper

Model Complexes. 2. Comparison of Three- and Four-Coordinate

Cu(II)-Thiolate Complexes and Fungal Laccase

David W. Randall,^†Serena DeBeer George,^†Patrick L. Holland,^‡Britt Hedman,^†,§

Keith O. Hodgson,^†,§William B. Tolman,*^,‡and Edward I. Solomon*^,†

Contribution from the Department of Chemistry, Stanford UniVersity, 333 Campus DriVe,

Stanford, California 94305, Department of Chemistry and Center for Metals in Biocatalysis,

UniVersity of Minnesota, 207 Pleasant Street SE, Minneapolis, Minnesota 55455, and Stanford

Synchrotron Radiation Laboratory, Stanford Linear Accelerator Center, Stanford UniVersity,

Stanford, California 94309

ReceiVed May 9, 2000

Abstract: To evaluate the importance of the axial ligand in blue Cu centers, the electronic structure of a

three-coordinate model compound LCuSCPh₃(2, L ) â-diketiminate ligand) is defined using low-temperature

absorption, magnetic circular dichroism (MCD), X-ray absorption spectroscopy (XAS), and resonance Raman

(rR) profiles coupled with density functional calculations. Using these excited-state spectroscopic methods the

electronic structure of 2 is compared to that of a four-coordinate blue Cu model compound LCuSCPh₃(1, L

) tris(pyrazolyl)hydroborate ligand) and the three-coordinate blue Cu center in fungal laccase. The spectral

features of 2 are substantially altered from those of 1 and reflect a trans influence of the â-diketiminate ligand

2

that involves a strong interaction with the Cu d_{x -y}orbital, concomitant with a decreased S pπ interaction

2

with the Cu d_{x -y}orbital. The lack of an axial ligand coupled with the influence of this equatorial donor leads

to many of the perturbed spectral features of 2 relative to 1 including: the shift of the S pπ f Cu CT transition

to lower energy and its reduced intensity, the stronger ligand field, the larger nitrogen covalency in the HOMO

at the expense of thiolate covalency, and the decreased excited-state distortion. From XAS, it also is clear that

loss of the axial pyrazole ligand in 2 relative to 1 leads to an increase in the effective nuclear charge of the

three-coordinate Cu in 2, which demonstrates that the axial ligand modulates the electronic structure. From a

comparison of 2 to fungal laccase it is evident that even in the absence of an axial ligand the electronic

structure can be modulated by differential charge donation from the equatorial ligands. These studies show

that elimination of the axial ligand of the blue copper site can affect the covalency of the thiolate-Cu bond

and potentially modify the electron-transfer properties of the site.

1. Introduction

(Cys), form a trigonal plane. The Cu-S(Cys) bond is very short

(2.1 Å), while the Cu-N(His) interactions are fairly typical (2.0

Å). The fourth ligand, S(Met), in the ligation sphere of the

prototypical blue Cu site is very long (Cu-S ≈ 2.8 Å).¹⁰Within

the diverse array of blue Cu proteins, the strength of this axial

ligand interaction shows considerable variability, which provides

a possible mechanism for adjusting the properties of the site

and thereby influencing reactivity. There are three general

classes of axial ligand interactions in blue Cu proteins. The first

includes a continuum of tetragonally distorted protein sites where

the axial Cu-thioether bond length decreases and is coupled

to a weakened Cu-thiolate bond and rotation of the S-Cu-S

plane relative to the N-Cu-N plane.^11,12In the second class,

which is typified by stellacyanin, the axial ligand is changed to

the stronger O(Gln) ligand, which leads to a tetrahedral distortion

of the site.^11,13In the third class, which is exemplified by the

Blue Cu proteins^1-4are important in both intra- and inter-

protein biological electron transfer (ET).^5-8The prototypical

blue, or type 1, Cu center in plastocyanin, which is important

in photosynthesis, is characterized by a trigonally distorted

tetrahedral geometry,^9,10where three strong ligands, N(His)₂S-

* To whom correspondence should be addressed. Fax: (650) 725-0259.

E-mail: Edward.Solomon@stanford.edu.

^†Department of Chemistry, Stanford University.

^‡University of Minnesota.

^§Stanford Synchrotron Radiation Laboratory, Stanford Linear Accelerator

Center, Stanford University.

(1) Baker, E. N. In Encyclopedia of Inorganic Chemistry; King, R., Ed.;

Wiley: Chichester, 1994; pp 883-905.

(2) Adman, E. T. AdV. Protein Chem. 1991, 42, 145-197.

(3) Sykes, A. G. AdV. Inorg. Chem. 1991, 36, 377-408.

(4) Solomon, E. I.; Baldwin, M. J.; Lowery, M. D. Chem. ReV. 1992,

92, 521-542.

(5) Nocek, J. M.; Zhou, J. S.; DeForest, S.; Priyadarshy, S.; Beratan, D.

N.; Onuchic, J. N.; Hoffman, B. M. Chem. ReV. 1996, 96, 2459-2489.

(6) Gray, H. B.; Winkler, J. R. Annu. ReV. Biochem. 1996, 65, 537-

561.

(7) Ullmann, G. M.; Knapp, E. W.; Kostic, N. M. J. Am. Chem. Soc.

1997, 119, 42-52.

(8) Sigfridsson, K. Photosyn. Res. 1998, 57, 1-28.

(9) Colman, P. M.; Freeman, H. C.; Guss, J. M.; Murata, M.; Norris, V.

A.; Ramshaw, J. A. M.; Venkatappa, M. P. Nature 1978, 272, 319-324.

(10) Guss, J. M.; Bartunik, H. D.; Freeman, H. C. Acta Crystallogr. 1992,

B48, 790-811.

(11) LaCroix, L. B.; Randall, D. W.; Nersissian, A. M.; Hoitink, C. W.

G.; Canters, G. W.; Valentine, J. S.; Solomon, E. I. J. Am. Chem. Soc.

1998, 120, 9621-9631.

(12) Randall, D. W.; Gamelin, D. R.; LaCroix, L. B.; Solomon, E. I. J.

Biol. Inorg. Chem. 2000, 5, 16-29.

(13) Hart, P. J.; Nersissian, A. M.; Herrmann, R. G.; Nalbandyan, R.

M.; Valentine, J. S.; Eisenberg, D. Protein Sci. 1996, 5, 2175-2183.

Published on Web 11/08/2000

Cu(II)-Thiolate Complexes and Fungal Laccase

J. Am. Chem. Soc., Vol. 122, No. 47, 2000 11633

the ligating S(Cys) in blue Cu centers. Complex 2 also differs

from the trigonal site in fungal laccase in that the â-diketiminate

ligand is used, which permits an evaluation of the influence of

equatorial ligands other than N(His) (or the closely related

N(pz)). To systematically evaluate the change in electronic

structure between the blue Cu center and complex 2, it is

important to separate the influences of the thiolate ligand from

those of the â-diketiminate nitrogen ligand. Comparing 2 to 1,

which both incorporate the same thiolate ligand, isolates the

electronic structural effects of the thiolate ligand from those of

the nitrogen ligand and permits an evaluation of the importance

of axial ligation.

In this work, a multifaceted, excited-state spectroscopic

analysis incorporating absorption, magnetic circular dichroism

(MCD), resonance Raman (rR), and X-ray absorption spectros-

copy (XAS) methodologies is coupled with density functional

theory (DFT) calculations to characterize the electronic structure

of 2. The electronic structure of 2 is compared with the

electronic structure of 1 that was defined by parallel studies in

the accompanying paper.²⁰Absorption and MCD spectroscopies

provide a method to distinguish the ligand field transitions from

the charge-transfer transitions, which provides insight into

changes in the ligand field environment. A vibrational analysis

of an isotopically labeled complex, 3 (Figure 1), related to 2

assists in assigning the Raman spectrum. Time-domain analysis

of the Raman profile data quantitates the excited-state Cu-S

bond length distortion associated with the charge-transfer

transition. XAS provides insight into the nature of the ground-

state wave function and comparison with 1 provides an estimate

of the relative effective nuclear charges (Z_eff) of Cu. DFT

calculations indicate important factors affecting the copper-

thiolate bonding interaction and the importance of the axial

ligand Finally, the electronic structure determined from the

spectroscopic analysis of 2 is compared to that of the naturally

occurring trigonal Cu S(Cys) thiolate center in fungal laccase.

Figure 1. Biological and synthetic Cu(II) thiolates. The blue Cu center

in fungal laccase (PDB Code: 1A65). Complex 1, [HB(pz′)₃]CuSCPh₃;

complex 2, (â-diketiminate)CuSCPh₃; and complex 3, (â-diketiminate)-

CuSC₆H₃Me₂.

type 1 center in fungal laccase, the axial ligand is absent.¹⁴Thus,

the role of the axial ligand in tuning the electronic structure is

an important issue for blue Cu centers.^12,15-18

A small-molecule model complex (2) (Figure 1) that has been

recently prepared¹⁹reproduces the uncommon trigonal Cu(II)

geometry present in the oxidized fungal laccase type 1 Cu site¹⁴

(Figure 1). Complex 2 incorporates a bidentate â-diketiminate

nitrogen ligand with 1.9 Å Cu-N bonds and a triphenylmethyl-

thiolate with a 2.1 Å Cu-thiolate bond,¹⁹similar to the

analogous distances in fungal laccase.¹⁴Direct comparison of

the electronic structures of the trigonal, three-coordinate Cu(II)

sites in 2 and fungal laccase is complicated by the fact that the

thiolate ligands are different: triphenylmethylthiolate in 2 versus

cysteinate in fungal laccase. In the accompanying paper²⁰the

differences in the electronic structure associated with this change

in the thiolate ligand are addressed by comparing the spectro-

scopically defined electronic structure of the prototypical blue

Cu site in plastocyanin^21,22to that of a tris(pyrazolyl)hydrobo-

rate-supported model complex, 1, that incorporates this thiolate

(Figure 1).^23-25From this study, the ligating S atom in

triphenylmethylthiolate is shown to be a stronger donor than

2. Experimental Procedures

2.1. Compounds. Published syntheses of 1, 2, and LCuCl (L )

â-diketiminate ligand shown in Figure 1) were used.^19,24All synthetic

procedures were performed in an inert-atmosphere glovebox or using

standard Schlenk techniques. The sodium salt of 2,6-dimethylphen-

ylthiol was prepared by adding the thiol (1 mL, 7.5 mmol) to a slurry

of sodium hydride (455 mg) in THF (20 mL), concentrating to 5 mL,

filtering, and precipitating with pentane (10 mL) to yield a white solid

consisting of the sodium thiolate and solvated THF (∼0.5 equiv by ¹H

NMR spectroscopy).

(14) Ducros, V.; Brzozowski, A. M.; Wilson, K. S.; Brown, S. H.;

Ostergaard, P.; Schneider, P.; Yaver, D. S.; Pedersen, A. H.; Davies, G. J.

Nat. Struct. Biol. 1998, 5, 310-316.

2.1.1. Preparation of 3. A solution of NaSC₆H₃(CH₃)₂‚¹/₂THF (25

mg, 0.13 mmol) in THF (3 mL) was added slowly to a red-purple

slurry of LCuCl (66 mg, 0.13 mmol) in THF (10 mL). The resultant

deep blue solution was stirred for 30 min and then slowly dried in

vacuo. The residue was extracted with pentane (10 mL), filtered through

a plug of Celite, and concentrated to 5 mL. This solution was cooled

overnight to give crystals of 2 (20 mg, 25% yield). UV-vis (pentane)

[λ_max, nm (ꢀ, mM^-1cm^-1)]: 340 (∼29), 458 (2.1), 729 (6.4); EPR (9.61

GHz, toluene, 20 K): g_|) 2.18, A_|) 115 × 10^-4cm^-1, g ) 2.04,

(15) Palmer, A. E.; Randall, D. W.; Xu, F.; Solomon, E. I. J. Am. Chem.

Soc. 1999, 121, 7138-7149.

(16) Xu, F.; Berka, R. M.; Wahleithner, J. A.; Nelson, B. A.; Shuster, J.

R.; Brown, S. H.; Palmer, A. E.; Solomon, E. I. Biochem. J. 1998, 334,

63-70.

(17) Lowery, M. D.; Solomon, E. I. Inorg. Chim. Acta 1992, 200, 233-

243.

(18) Olsson, M. H. M.; Ryde, U. J. Biol. Inorg. Chem. 1999, 4, 654-

663.

(19) Holland, P. L.; Tolman, W. B. J. Am. Chem. Soc. 1999, 121, 7270-

7271.

(20) Randall, D. W.; George, S. D.; Hedman, B.; Hodgson, K. O.;

Fujisawa, K.; Solomon, E. I. J. Am. Chem. Soc. 2000, 122, 11620-11631.

(21) Gewirth, A. A.; Solomon, E. I. J. Am. Chem. Soc. 1988, 110, 3811-

3819.

(22) LaCroix, L. B.; Shadle, S. E.; Wang, Y. N.; Averill, B. A.; Hedman,

B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1996, 118, 7755-

7768.

A

) 13 × 10^-4cm^-1(simulated with QPOWA²⁶); Anal. Calcd for

C₄₈H₅₆CuSN₂: C, 71.86; H, 8.15; N, 4.53. Found: C, 71.80; H, 8.30;

N, 4.58. The X-ray crystal structure of 3 is presented in the Supporting

Information. Important crystallographic data: monoclinic, space group

P2₁/c, a ) 11.3523(2) Å, b ) 17.0133(3) Å, c ) 18.3511(2) Å, â )

103.490(1)°, V ) 3446.55(9) Å³, Z ) 4, F_calcd) 1.192 g/cm³. Non-

hydrogen atoms were refined with anisotropic thermal parameters, and

(23) Kitajima, N.; Fujisawa, K.; Moro-oka, Y. J. Am. Chem. Soc. 1990,

112, 3210-3212.

(26) (a) M. J. Nilges, Ph.D. Thesis, University of Illinois, Urbana, Illinois,

1979. (b) Belford, R. L.; Nilges, M. J. “Computer Simulation of Powder

Spectra”, EPR Symposium, 21st Rocky Mountain Conference, Denver,

Colorado, August, 1979. (c) A. M. Maurice, Ph.D. Thesis, University of

Illinois, Urbana, Illinois, 1980.

(24) Kitajima, N.; Fujisawa, K.; Tanaka, M.; Moro-oka, Y. J. Am. Chem.

Soc. 1992, 114, 9232-9233.

(25) Qiu, D.; Kilpatrick, L. T.; Kitajima, N.; Spiro, T. G. J. Am. Chem.

Soc. 1994, 116, 2585-2590.

11634 J. Am. Chem. Soc., Vol. 122, No. 47, 2000

Randall et al.

hydrogen atoms were in idealized positions with riding thermal

parameters. Full-matrix least squares refinement on F²converged with

R1 ) 0.0295, wR²) 0.0727, GOF ) 1.033 for 4760 independent

reflections (I > 2σ(I)) and 382 parameters.

2.5. X-ray Absorption Spectroscopy Measurements and Data

Analysis. All data were measured at the Stanford Synchrotron Radiation

Laboratory under ring conditions 3.0 GeV and 60-100 mA.

S K-edge data were measured using the 54-pole wiggler beam line

6-2 in high magnetic field mode of 10 kG with a Ni-coated harmonic

rejection mirror and fully tuned Si(111) double crystal monochromator.

Details of the optimization of this setup for low-energy studies have

been described in an earlier publication.³⁴S K-edge measurements were

made at room temperature. Samples were ground into a fine powder

and dispersed as thinly as possible on Mylar tape to minimize the

possibility of self-absorption. The data were measured as fluorescence

excitation spectra utilizing an ionization chamber as a fluorescence

detector.^35,36To check for reproducibility, 2-3 scans were measured

for each solid sample. The energy was calibrated from S K-edge spectra

of Na₂S₂O₃‚5H₂O, run at intervals between sample scans. The maximum

of the first preedge feature in the spectrum was assigned to 2472.02

eV. Data were averaged, and a smooth background was removed from

all spectra by fitting a polynomial to the preedge region and subtracting

this polynomial from the entire spectrum. Normalization of the data

was accomplished by fitting a flattened polynomial or straight line to

the postedge region and normalizing the edge jump to 1.0 at 2490 eV.

Fits to the edges were performed using the program EDG_FIT.³⁷Second

derivative spectra were used as guides to determine the number and

position of peaks. Preedge and rising edge features were modeled by

pseudo-Voigt line shapes. For the preedge feature, a fixed 1:1 ratio of

Lorentzian to Gaussian contributions was used. Fits were performed

over several energy ranges. The reported intensity values and standard

deviations are based on the average of all good fits. Normalization

procedures can introduce ∼3% error in preedge peak intensities, in

addition to the error resulting from the fitting procedure.

Cu L-edge data were measured using the 31-pole wiggler beam line

10-1. Samples were finely ground and spread across double-adhesive

conductive carbon tape, which was attached to an aluminum paddle.

The data were measured at room temperature as total electron yield

spectra utilizing a Galileo 4716 channeltron electron multiplier as a

detector. For each sample, 3-4 scans were measured to check

reproducibility. The energy was calibrated from the Cu L-edge spectra

of CuF₂, run at intervals between sample scans. The maximum of the

L₃and L₂preedges were assigned to 930.5 and 950.5 eV, respectively.

A linear background was fit to the preedge region (870-920 eV) and

was subtracted from the entire spectrum. Normalization was ac-

complished by fitting a straight line to the postedge region and

normalizing the edge jump to 1.0 at 1000 eV. Fits to the edges were

performed using EDG_FIT.³⁷A pseudo-Voigt peak was used to model

the L₃and L₂2p f 3d transitions. Arctangent functions were used to

model the L₃and L₂edge jumps. The total L-preedge intensity reported

here was calculated as L₃+ L₂. The reported intensity values and

standard deviations are based on the average of all good fits.

Normalization procedures can introduce ∼4% error in preedge peak

intensities, in addition to the error resulting from the fitting procedure.

2.6. Calculations. Density functional theory (DFT) calculations were

performed using the Amsterdam Density Functional package of

Baerends and co-workers (ADF 2.0.1) using the database IV basis

set.^38,39The Vosko, Wilk, Nusair local density approximation⁴⁰was

used for exchange and correlation, respectively. Generalized gradient

2.1.2. Sulfur-34 Labeling. Preparation of ³⁴S-enriched 2,6-dimeth-

ylphenylthiol was accomplished by addition of solid sulfur-34 (45 mg,

1.3 mmol, 77% atomic enrichment, Cambridge Isotopes) to a solution

of 2,6-dimethylphenyl magnesium bromide (1.0 mL, 1.0 M in THF,

Aldrich) at room temperature. This solution was stirred under nitrogen

for 3 h, and then lithium aluminum hydride (∼0.1 g) was added, causing

the pale yellow color to fade. The reaction was quenched with saturated

NH₄Cl (50 mL), and the aqueous layer was extracted with three portions

of 25 mL of diethyl ether. The combined organic layers were dried

over MgSO₄, reduced to an oil, and distilled at 45 °C (0.1 mmHg) to

yield a sample of labeled 2,6-dimethylphenylthiol that was used to make

the sodium salt (as described above) without further manipulation.

Synthesis of isotopically labeled complex 3 was accomplished using

procedures similar to those described above.

2.2. UV-Vis Absorption and MCD. Room-temperature absorption

spectra were recorded in heptane, pentane, or toluene on a HP8453

diode-array spectrophotometer. Low-temperature UV-vis absorption

spectra were recorded at ∼10 K using either a Cary 500 or Cary 17

equipped with a Janis Supervaritemp dewar. MCD spectra were

recorded using Jasco J500 (or J810, UV-visible, PMT detection) and

J200 (near-IR, liquid nitrogen-cooled InSb solid-state detection) spec-

tropolarimeters modified to include Oxford SM-4 (7 T, UV-vis) or

SM-4000 (7 T, near-IR) superconducting magnets with optical access

within their sample compartments. Special care was taken to provide

magnetic shielding for the PMT detector. For low temperature MCD

experiments, solid samples (mulls) that were prepared by finely grinding

microcrystalline material into powders with a mortar and pestle and

then adding mulling agents (poly(dimethylsiloxane) (Aldrich) or

Fluorolube (Wilmad)) were uniformly spread between quartz disks

(Heraeus-Amersil) and loaded into copper MCD cells and promptly

frozen in liquid nitrogen.

2.4. Raman and Resonance Raman Enhancement Profiles. In

initial rR spectra and sulfur-34 labeling experiments performed at

Minnesota, resonance Raman spectra were collected on an Acton 506

spectrometer using a Princeton Instruments LN₂/CCD-1100-PB/UVAR

detector and ST-1385 controller, equipped with a 1200 grooves/mm

holographic grating, interfaced with Winspec software. A grating with

2400 grooves/mm was used for confirmation of the small ³⁴S isotope

shifts, and the shifts reported here are deemed accurate to 1 cm^-1. A

Spectra-Physics 2030-15 Ar ion laser at a power of 4 W was employed

to pump a 375B CW dye (Rhodamine 6G) laser at 632.8 nm. Solutions

(∼50 mM, d₆-benzene) were frozen onto a gold-plated copper coldfinger

in thermal contact with a dewar containing liquid nitrogen. The spectra

were obtained at 77 K using a 135° backscattering geometry. Raman

shifts were referenced externally through a quadratic fit to the known

spectrum of indene at room temperature.²⁷

At Stanford, (resonance) Raman spectra were recorded using a

Princeton Instruments, liquid nitrogen cooled, back-illuminated CCD

camera mounted on a Spex 1877 0.6 m triple spectrometer, equipped

with 1200, 1800, or 2400 grooves/mm holographic gratings. Continuous

wave Coherent Kr ion (Innova 90C-K) and Ar ion (Sabre-25/7) visible

and UV laser lines were used for variable-energy excitation. A

polarization scrambler was placed in front of the entrance slits of the

spectrometer. Samples were loaded in 5-mm (o.d.) NMR tubes

immersed in liquid nitrogen, and spectra were obtained in a ∼135°

backscattering geometry with ∼40 mW incident power. Raman

scattering resolution and accuracy is ∼2 cm^-1. Raman peak profile

intensities were determined relative to normal Raman scattering of

solvent peaks. Resonance Raman enhancement profiles (RREPs) were

simulated using the time-dependent theory of Heller, et al.^28-32that

was implemented in a MathCAD script.³³The parameters of the fits

were adjusted until the simulated spectra reasonably matched the

experimental data. The same set of parameters was used to simulate

both the resonance Raman enhancement profile and the absorption

spectrum.

(28) Heller, E. J. Acc. Chem. Res. 1981, 14, 368-375.

(29) Heller, E. J.; Sundberg, R. L.; Tannor, D. J. Phys. Chem. 1982, 86,

1822-1833.

(30) Myers, A. B.; Mathies, R. A. In Biological Applications of Raman

Spectroscopy; Spiro, T. G., Ed.; Wiley: New York, 1987; Vol. 2, pp 1-58.

(31) Myers, A. B. Acc. Chem. Res. 1997, 30, 519-527.

(32) Zink, J. I.; Shin, K. S. K. AdV. Photochem. 1991, 16, 119-214.

(33) Brunold, T. C.; Tamura, N.; Kitajima, N.; Moro-oka, Y.; Solomon,

E. I. J. Am. Chem. Soc. 1998, 120, 5674-5690.

(34) Hedman, B.; Frank, P.; Gheller, S. F.; Roe, A. L.; Newton, W. E.;

Hodgson, K. O. J. Am. Chem. Soc. 1988, 110, 3798-3805.

(35) Stern, E. A.; Heald, S. M. ReV. Sci. Instrum. 1979, 50, 1579-1582.

(36) Lytle, F. W.; Greegor, R. B.; Sandstrom, D. R.; Marques, E. C.;

Wong, J.; Spiro, C. L.; Huffman, G. P.; Huggins, F. E. Nucl. Instrum.

Methods 1984, 226, 542-548.

(37) George, G. N. EDG_FIT; Stanford Synchrotron Radiation Labora-

tory, Stanford Linear Accelerator Center, Stanford University, Stanford,

CA 94309.

(27) Methods in Enzymology; Riordan, J. F.; Vallee, B. L., Eds.;

Academic Press: New York, 1993; Vol. 226, p 351.

Cu(II)-Thiolate Complexes and Fungal Laccase

J. Am. Chem. Soc., Vol. 122, No. 47, 2000 11635

approximations of Becke⁴¹and Perdew⁴²were included for exchange

and correlation. The calculations reported here are for spin-restricted

systems; however, spin-unrestricted calculations gave very similar

results. Calculations were also attempted with the Gaussian 98 package

using the B3LYP functional⁴³and the SCF-XR-SW package.⁴⁴How-

ever, these packages give a ground electronic state that is inconsistent

with experiment; a â-diketiminate ligand-based HOMO (π_nb,b1in Table

5) is calculated, rather than a Cu-based HOMO. For the B3LYP

calculations, several basis sets, including many with different degrees

of polarization, all gave the π_nb,b1ground state. To model the geometry

of 2, only the essential C₃H₅N₂^-core of the â-diketiminate ligand was

retained. Likewise, the thiolate was approximated by SCH₃^-. The

calculations on the resulting [C₃H₅N₂CuSCH₃]⁰complex were done

single point at the X-ray structure, but symmetrized to C_s. Thus, the

small deviation of the Cu from the N₂S plane was retained. Input files,

including the atomic coordinates, are included in the Supporting

Information.

3. Results and Analysis

3.1. Synthesis and Characterization of a 3-Coordinate Aryl

Thiolate Complex. Using synthetic methods analogous to those

used for 2,¹⁹a 3-coordinate â-diketiminate Cu(II) complex of

the 2,6-dimethylphenylthiolate ligand was prepared. The X-ray

crystal structure of this product, 3, is presented in the Supporting

Information. The geometry of 3 is very similar to that of 2,

with the copper atom lying only 0.1046(7) Å from the N₂S

plane, demonstrating its trigonal coordination sphere. Most

notable are the small differences in bond angles and lengths,

some of which are attributable to the lesser steric demands of

the aryl group versus the triphenylmethyl group. For example,

the Cu-S-C angle is substantially smaller (107.63(7)° in 3

versus 119.43(8)° in 2), and the S-C (1.789(2) Å in 3 versus

1.883(2) Å in 2) and Cu-N (average 1.902 Å in 3 vs 1.922 Å

in 2) bonds are shorter. Interestingly, though, the Cu-S bond

is longer (2.1382(5) in 3 vs 2.1243(8) in 2), pointing to a “push-

pull” effect between the thiolate and the â-diketiminate ligand;

this theme will be elaborated at length below.

Despite these structural modifications, the substitution of an

aryl group in 3 for the alkyl group of 2 causes only minimal

changes in the electronic absorption and EPR spectra. Thus the

intense low-energy charge-transfer absorption (vide infra) lies

at 729 nm in 3 (749 nm in 2), and the EPR spectrum of 3 is

nearly superimposable on that of 2. Because of these similarities,

compound 3 will be discussed below only in the context of

resonance Raman spectroscopy, where it was possible to use

the ³⁴S-labeled form of 3 to identify vibrations involving Cu-S

stretching.

Figure 2. Excited-state electronic spectra of complex 2, (â-diketimi-

nate)CuSCPh₃in heptane in comparison to complex 1, [HB(pz′)₃]-

CuSCPh₃. (A) Room-temperature absorption spectrum of 2, including

an overlay of Gaussian fits summarized in Table 1. (B) Low-temperature

(5 K) magnetic circular dichroism (MCD) spectrum of 2 at a field of

7 T, including Gaussian fits summarized in Table 1.

Table 1. Experimental MCD and Absorption Band

Characterization for 2

band assignment energy (cm^-1) ꢀ (M^-1cm^-1) osc str MCD/ABS^a

2

1

2

3

4

5

6

7

8

9

d_z

6300

∼9000

13500

16100

18200

20450

22800

24700

28500

s

5400

780

1200

1210

880

740

16360

nd

+ve

-ve

3.2. Absorption and Magnetic Circular Dichroism Spec-

troscopy.

π_nb,b1

S pπ CT

d_xy

0.0553 -0.018

0.0081 -0.075

0.0123 +0.110

0.0124 -0.057

0.0090 -0.027

0.0076 +0.045

0.1009 nd

3.2.1. Absorption. As demonstrated in Figure 2A and

summarized in Table 1, the absorption spectrum of 2 is

characterized by an intense, low-energy transition at ∼750 nm

() 13500 cm^-1; ꢀ ≈ 5400 M^-1cm^-1) (band 3).¹⁹Between

15000 and 25000 cm^-1there are several weaker bands (bands

4-8, ꢀ < 1200 M^-1cm^-1). At 28500 cm^-1lies intense (ꢀ ≈

16400 M^-1cm^-1) band 9. Gaussian fits that are simultaneously

consistent with both the absorption spectrum and the low-

temperature MCD spectrum (vide infra) are included in the

d_yz+xz

d_yz-xz

S p ps.σ

π_a2

Lig π f π*

^aRatio of MCD intensity to absorption intensity. This ratio ap-

proximates the relative C/D ratios for mull data, where it is impossible

to obtain absolute C/D ratios.

figure and summarized in Table 1. The low-temperature mull

absorption spectrum (not shown) is similar in general appearance

to that shown in Figure 2A.

3.2.2. MCD. The low-temperature MCD spectrum of a poly-

(dimethylsiloxane) mull of 2 is presented in Figure 2B. Fits to

the spectrum are summarized in Table 1. At the low tempera-

tures employed in these experiments, the MCD intensity

originates exclusively from a C-term mechanism as determined

(38) ADF 2.0.1; Vrije Universiteit, Theoretical Chemistry, De Boelelaan

1083, 1081 HV Amsterdam, The Netherlands, 1995.

(39) te Velde, G.; Baerends, E. J. J. Comput. Phys. 1992, 99, 84-98.

(40) Vosko, S. H.; Wilk, L.; Nusair, M. Can. J. Phys. 1980, 58, 1200-

1211.

(41) Becke, A. D. Phys. ReV. A 1988, 38, 3098-3100.

(42) Perdew, J. P. Phys. ReV. B 1986, 33, 8822-8824.

(43) Becke, A. D. J. Chem. Phys. 1993, 98, 5648-5652.

(44) Cook, M.; Case, D. A. QCPE Program #465, 1991; Vol. 23.

11636 J. Am. Chem. Soc., Vol. 122, No. 47, 2000

Randall et al.

Table 2. Oscillator Strengths for S pπ f Cu CT Band

from the temperature dependence of the MCD spectral intensity;

that is, C (âB/kT) ∆ꢀ, where â is the Bohr magneton, B is

the magnetic field, k is the Boltzmann constant, T is the

temperature (K), and ∆ꢀ is the molar circular dichroism. The

saturation behavior of the features in the low-temperature MCD

spectra gives a g_isovalue of 2.10, consistent with EPR,¹⁹though

the latter technique better resolves the anisotropy of the

g-interaction. A moderately intense MCD band (Figure 2B, band

1) is observed at low energy, 6300 cm^-1. Band 2 is observed at

∼9000 cm^-1. An MCD feature (band 3) is observed at the same

energy as the strong 750 nm absorption (13500 cm^-1). Of

particular importance are the three intense MCD bands (bands

4-6) to higher energy than the 750 nm absorption (band 3). In

the spectrum shown in Figure 2B, the MCD features in the

28000-30000 cm^-1region (bands 9 and above) are distorted

due to the strong absorptions in this region. However, a spectrum

obtained on a more dilute mull, where this issue is alleviated,

does not show significant MCD intensity in this region (not

shown).

compound

1

2

osc. strength f_exp

0.0777^a

16000

0.0777

0.0553^a

13500

0.0664

S pπ f Cu CT transition freq/cm^-1

freq. scaled f_{exp, sc}

^aFrom room-temperature absorption spectra.

Raman data (vide infra) band 9 is assigned as an intraligand π

f π* transition.

3.2.4. Comparison to 1. Many features in the optical spectra

of 2 that are presented in Figure 2 are different than those of

1,²⁰in particular, and those of other highly covalent Cu-thiolate

centers.^11,15,21,22As Figure 2A indicates, relative to complex 1,

the intense, low-energy S pπ f Cu CT band (band 3) is shifted

to even lower energy in 2: from 16000 cm^-1(625 nm) in 1 to

13500 cm^-1(750 nm) in 2. The energy shift of the CT band is

also clear from the MCD spectrum (Figure 2B). The ligand field

bands in 2, which are intense in MCD but weak in absorption,

are analogous to the ligand field bands at lower energy than

the intense 600 nm band in 1. However, there is a striking

difference in the energies of these ligand field bands between

2 and 1. Figure 2B demonstrates that bands 4, 5, and 6, which

move in concert, are to much higher energy in 2 relative to 1,

for example, the highest energy d-d band moves from 11080

cm^-1in 1 to 20450 cm^-1in 2. This substantial shift of the d-d

bands to higher energy clearly indicates that the ligand field is

much stronger in 2. The low-energy band (band 1) in 2 is

analogous to the 5200 cm^-1band in 1, though it is shifted to

significantly higher energy (∼1100 cm^-1). This band corre-

3.2.3. Band Assignments. The bands in 2 can be assigned

in analogy with those in 1, corresponding spectra for which are

included in Figure 2 for comparison,²⁰and the blue Cu center

in plastocyanin (the coordinate system is given in Figure 1,

where z is perpendicular to the S(thiolate)N₂plane and x and y

are bisected by the S(thiolate)-Cu bond).^21,22For a system like

2, MCD intensity derives from out-of-state spin-orbit coupling

to energetically nearby states. The magnitude of such spin-

orbit coupling scales with the spin-orbit coupling constant ê,

which is much larger for Cu (830 cm^-1) than for S (380 cm^-1

)

or N (70 cm^-1). This enables the use of MCD C-term band

intensities relative to absorption band intensities (i.e., C₀/D₀

ratios) to distinguish d f d (or ligand field) transitions, which

have strong MCD intensity, from charge-transfer (CT) transi-

tions, which have weaker MCD intensity.²¹The large MCD

intensity of bands 4-6 that are clustered around 18500 cm^-1

in Figure 2B, coupled with their low absorption intensity from

Figure 2A (the MCD/Abs ratio, Table 1, for these bands is ∼4

times larger than for band 3), enables us to assign these bands

as d-d bands. Likewise, the low-energy band 1 is assigned as

the fourth d-d band. The specific LF bands are assigned in

analogy with those in 1²⁰and the blue Cu center in plastocya-

nin.^21,22The signs of the d f d MCD features in 2 are identical

2

sponds to a transition from the d_zorbital, which is lower in

energy in 2 due to the absence of an axial ligand. This decreases

the antibonding interaction along the z-axis and allows the

2

4s/d_zmixing to increase. Finally, there are no counterparts in

complex 1 for band 2 at ∼9000 cm^-1and band 9 at 28500 cm^-1

,

confirming their association with the â-diketiminate donor

ligand.

Comparison of the intensities of the low energy S pπ f Cu

CT bands in 1 and 2 (Figure 2A) reveals a further difference

between 1 and 2. Quantitatively, the band intensity can be

expressed by its oscillator strength, f. To determine the oscillator

strengths from the experimental data we use the approxima-

tion: f_exp) 4.61 × 10^-9ꢀ_max

ν_1/2, where ꢀ_maxis the maximum

to those in plastocyanin.²¹At lowest energy is Cu d_z(band 1,

2

absorption and ν_1/2is the full-width at half-maximum of the

peak. The experimental oscillator strengths are 0.077 and 0.055

for 1 and 2, respectively (see Table 2). Oscillator strengths give

positive), while Cu d_xy(band 4, negative), Cu d_yz-xz(band 5,

positive), and Cu d_yz+xz(band 6, negative), in order of increasing

transition energy, lie to higher energy than band 3.

a measure of the transition moment⁴⁶(f(ν) ν‚|‚ψ_i|µ|ψ_f| ) and

2

The significant absorption intensity of band 3, the smaller

MCD/Abs ratio (0.02, Table 1) than bands 4-6 (0.08 ( 0.03),

Raman profile data (vide infra), and density functional calcula-

tions (vide infra) indicate that this low-energy, intense transition

is the S pπ f Cu CT transition. Band 2 is associated with the

â-diketiminate ligand and will be considered later, as will the

assignment of the weak bands 7 and 8. Possibilities for the latter

set include N f Cu CT and the S (pseudo-σ) f Cu CT

transitions. High energy, intense band 9 is associated with the

â-diketiminate N-donor ligand, since the absorption spectrum

of spectroscopically transparent lithium, thallium(I), and copper-

(I) â-diketiminates also show an intense absorption near 350

nm, suggesting that this absorption is general to complexes

containing the â-diketiminate ligand.⁴⁵The lack of significant

MCD intensity in band 9 further supports the ligand-based

assignment for this band, as the C-term MCD intensity will scale

with the small ê values of N and C, relative to Cu. Based on

have an intrinsic ν dependence (i.e., for a constant transition

moment the transition intensity f increases with transition

energy). Even when the oscillator strength of 2 is scaled by the

ratio of the transition frequencies to take this factor into account,

the resulting transition moment of 2 is only 86% that of 1 (Table

2). Since absorption intensity is proportional to overlap of the

ligand orbitals in the donor and acceptor orbitals involved in

the electronic transition, the reduced oscillator strength of 2

compared to 1 points to less S pπ ligand character in the ground-

state wave function (i.e., HOMO) of 2.

3.3. Resonance Raman Spectroscopy.

3.3.1. Vibrations and Isotopic Substitution. Raman spectra

of 1²⁵and 2¹⁹have been reported previously. Figure 3A

compares the resonance Raman (rR) spectra of 2 and 3 using

laser excitation into their 750 nm absorption bands and the rR

spectrum of 1 obtained using excitation into its 625 nm

absorption band. When excited into their S pπ-Cu CT bands,

(45) Holland, P. L.; Tolman, W. B. Unpublished work.

(46) Solomon, E. I. Comm. Inorg. Chem. 1984, 3, 225-320.

Cu(II)-Thiolate Complexes and Fungal Laccase

J. Am. Chem. Soc., Vol. 122, No. 47, 2000 11637

Figure 4. Raman spectrum of 3 in frozen (77 K) d₆-benzene showing

the effect of ³⁴S isotopic labeling; λ₀) 632.8 nm.

shift of 3 cm^-1is also observed for the 355 cm^-1band (shifts

of other bands are 1 cm^-1or less, see Table S1, Supporting

Information).

3.3.2. Assignments and Correlations with 1. The fact that

the ∼425 cm^-1vibrational band in all the complexes shows

such large enhancement upon excitation into their respective S

pπ-Cu CT bands suggests that this vibration be assigned as the

Cu-S stretch. The isotopically labeled Raman data in Figure 4

make this assignment unambiguously clear, since ³⁴S incorpora-

tion in 3 results in a 6 cm^-1shift of the 433 cm^-1peak to lower

frequency. This assignment parallels and confirms the assign-

ment of Spiro, et al. for 1 (and related complexes)²⁵and also

the general assignment for blue Cu proteins.^47-50The model

complexes studied here exhibit much less mechanical coupling

between the Cu-S stretch and thiolate side chain deformations

than in blue Cu proteins, in which this coupling yields their

characteristic vibrational envelope in the 350-450 cm^-1

region.^47-50In addition to the intense 433 cm^-1band, in 3 there

is also an intense band at 355 cm^-1. However, the substantial

enhancement of the 433 cm^-1overtone relative to the 355 cm^-1

overtone and combination bands, suggests that for complex 3,

the 433 cm^-1peak is a fairly pure Cu-S stretch. Raman spectra

of complexes 2 and 3 are rather similar to those of 1. In

particular, the Cu-S stretching frequency in all of these Cu-

(II)-thiolate compounds is quite similar and relatively high at

∼425 cm^-1. This indicates that 1, 2, and 3 have Cu-S bonds

with similar strengths, independent of the nitrogen ligand. The

small difference (7 cm^-1) between the Cu-S stretching frequen-

cies in 1 and 2 is consistent with small differences in the Cu-S

bond length:⁵¹2.12 Å in 2 versus 2.13 Å in 1.

Figure 3. Resonance Raman spectra of Cu(II) thiolate model systems

1 [HB(pz′)₃]CuSCPh₃, 2 LCuSCPh₃, and 3 LCuSC₆H₃Me₂, where L )

â-diketiminate. (A) rR spectra obtained using excitation (λ₀) 752 nm,

647 nm) into the respective S pπ f Cu CT transitions. The vibration

at ∼425 cm^-1corresponds to the Cu-S stretch, while vertical arrows

highlight the Cu-N vibration. Analogous vibrations in 1, 2, and 3 are

indicated by a, b, c, d, and e, as described in the text. (B) rR spectra

obtained using excitation (λ₀) 351 nm) into the high energy π-π*

transition. Black dots represent solvent vibrations; 2 and 3 in frozen

(77 K) d₆-benzene and 1 in frozen (∼120 K) toluene.

all complexes show an intense band at ∼425 cm^-1. In complex

1 this band is at 421 cm^-1, while in 2 it shifts to 428 cm^-1and

in 3 it is slightly higher still at 433 cm^-1(bands a, Figure 3A).

The band at 333 cm^-1in 2 appears to shift to 355 cm^-1in 3

and become more intense (bands c), while weaker bands at 256

and 297 cm^-1(bands d and e) are at essentially identical

frequencies in these two complexes. An apparent counterpart

to the 333 cm^-1band in 2 is observed in complex 1 at 324

cm^-1. Further, in the â-diketiminate-ligated complexes, a band

at 370 cm^-1in 2 shifts to 387 cm^-1in 3 (bands b). There is an

additional band at 209 cm^-1in 3 not present in 2; reciprocally,

a band at ∼145 cm^-1in 2 does not appear to have a counterpart

in 3. To higher Raman shift at this excitation energy (752 nm),

the most intense bands are combinations and overtones of the

fundamentals (not shown). For complex 3, which has two intense

bands in the 300-450 cm^-1region (355 and 433 cm^-1), the 2

ν_iovertone for the 433 cm^-1band is 5.2 times more intense

than the analogous overtone for the 355 cm^-1band. The effect

of ³⁴S isotopic substitution in 3 on the vibrational spectrum is

presented in Figure 4. The most obvious change in the rR

spectrum is a 6 cm^-1shift in the ∼433 cm^-1band. A smaller

The 333 cm^-1band in 2 that upshifts to 355 cm^-1in 3 seems

to be analogous to a band in 1 at 322 cm^-1. In 3, the only blue

Cu model complex where the thiolate sulfur has been labeled,

this band shows a small (3 cm^-^{1 34}S isotope shift relative to

)

the 6 cm^{-1 34}S isotope shift of the 433 cm^-1band. A Raman

(47) Blair, D. F.; Campbell, G. W.; Schoonover, J. R.; Chan, S. I.; Gray,

H. B.; Malmstro¨m, B. G.; Pecht, I.; Swanson, B. I.; Woodruff, W. H.; Cho,

W. K.; English, A. M.; Fry, H. A.; Lum, V.; Norton, K. A. J. Am. Chem.

Soc. 1985, 107, 5755-5766.

(48) Andrew, C. R.; Sanders-Loehr, J. Acc. Chem. Res. 1996, 29, 365-

372.

(49) Qiu, D.; Dong, S. L.; Ybe, J. A.; Hecht, M. H.; Spiro, T. G. J. Am.

Chem. Soc. 1995, 117, 6443-6446.

(50) Czernuszewicz, R. S.; Dave, B. C.; Germanas, G. P. In Spectroscopic

Methods in Bioinorganic Chemistry; Solomon, E. I., Hodgson, K. O., Eds.;

American Chemical Society: Washington, DC, 1998; pp 220-240.

(51) Herschbach, D. R.; Laurie, V. W. J. Chem. Phys. 1961, 35, 458-

463.

11638 J. Am. Chem. Soc., Vol. 122, No. 47, 2000

Randall et al.

of Cu-S or Cu-Cl stretches is observed). Further, the high

frequencies of the strongly enhanced vibrations are consistent

with intraligand C-N and/or C-C stretches, which implies that

the high intensity of these vibrations derives from considerable

distortion along these modes in the excited electronic state at

350 nm. This type of geometric distortion would be expected

for an excited electronic state with a π-antibonding interaction

between atoms in the â-diketiminate ligand, as would be

observed in a π* state. The fact that resonance Raman profiles

reveal that there is some Cu-N excited-state distortion in band

9 is also consistent with it being associated with a ligand π*

excited state. A transition from an orbital with intraligand

nonbonding C-C or C-N interactions to one with antibonding

interactions could modulate the strength of the Cu-N interac-

tion, leading to its Raman enhancement. These two arguments

strongly argue for assignment of the 350 nm band as an

intraligand π-π* transition.

3.3.3. Enhancement Profile Analysis and Excited-State

Distortion. The resonance Raman enhancement profile (RREP)

in Figure 5 shows the excitation wavelength dependence of the

Raman spectral intensity relative to an internal intensity standard,

in this case solvent bands. This excitation energy dependence

of the Raman spectrum is due to the that fact that resonance

Raman intensity derives from geometric distortions in the

excited electronic state.⁵²Since different excitation wavelengths

involve resonance with different excited electronic states (and

therefore different excited geometries), a different set of

vibrational bands can be enhanced with different excitation

energies. From Figure 5, the ∼425 cm^-1band, which has been

assigned above based on ³⁴S isotope shifts as the Cu-S(thiolate)

stretch, is strongly enhanced through band 3 (λ_max≈ 750 nm

≈ 13500 cm^-1) of 2. This vibration is expected to be strongly

enhanced in the S f Cu CT transition (band 3), since this

electronic transition formally involves promotion of an electron

from a bonding Cu-S pπ orbital to the HOMO where this

interaction is antibonding; leading to a large excited-state

distortion in the Cu-S bond. For bands 4-6 no resonance

enhancement is observed, consistent with their assignment as d

f d transitions at higher energy than the S pπ f Cu CT band.

Bands 7 and 8 show no resonance enhancement and the RREP

provides no further insight into their assignment. In contrast,

Figure 5. Heller fits of the absorption and resonance Raman enhance-

ment profiles (RREP) for complex 2 using the parameters in the text

and summarized in Table 3 for the S pπ f Cu CT band.

spectrum on an aryl thiolate analogue of 1, [HB(pz′)₃]CuSC₆F₅,

(Figure S1, Supporting Information) shows increased intensity

in two partially resolved features at ∼340 cm^-1and ∼350 cm^-1

,

in parallel to the higher frequency and intensity of the 355 cm^-1

band in the aryl thiolate complex, 3, (where R ) 2,6-

dimethylphenyl) relative to the alkyl thiolate 2 (where R )

triphenylmethyl). Given these spectroscopic observations, it

appears that in copper-thiolate systems utilizing an aryl thiolate,

this vibration(s) is at ∼20 cm^-1higher frequency and higher in

intensity than with an alkyl thiolate, independent of the nitrogen

ligand. This band is likely associated with a limited amount of

mechanical coupling of the Cu-S stretch with an internal aryl

thiolate ligand vibration involving S.

The excitation wavelength dependence of the Raman spec-

trum also aids in assigning the Raman spectra. Confirming that

they are indeed analogous, the 370 cm^-1band in 2 (Figure 5)

and the 386 cm^-1band in 3 (Figure S2) exhibit very similar

Raman enhancement profiles. Figures 5 and S2 demonstrate that

these vibrational bands show enhancement both in the low

energy (750 nm) CT absorption band as well as the higher

energy (350 nm) absorption. This observation is consistent with

the assignment of these vibrations as Cu-N stretches. The

HOMO of 2 has substantial N character, and therefore, some

distortion of the nitrogen ligands would be expected in the low

energy S pπ f Cu CT excited state (vide infra). The increase

in Cu-N frequency in 3 relative to 2 is consistent with the

shorter Cu-N distances (0.02 Å shorter) in the former. Complex

1 does not appear to have a counterpart to this Cu-N vibration

band. The weak, low-frequency features at 256 and 297 cm^-1

are at almost identical frequencies in 2 and 3, and therefore are

likely associated with internal â-diketiminate ligand modes.

Finally, the resonance Raman excitation profile in Figure 5

confirms the ligand π f π* assignment for the high energy

28500 cm^-1(350 nm) electronic transition (band 9) in Figure

2A. Specifically, the Raman spectra of complexes 2, 3, (Figure

3B) and the LCuCl starting material (not shown) are very similar

using 351 nm (28490 cm^-1) excitation energy. Figure 3B

demonstrates that the most intense vibrational features in these

spectra are at high frequency (545 cm^-1, ∼1300 cm^-1, and

∼1600 cm^-1). These observations confirm that this band is

independent of the thiolate (or Cl) ligand (since no enhancement

the â-diketiminate intraligand π-π* transition (band 9, λ_max

)

350 nm) shows substantial resonance enhancement, but a

different set of vibrational bands is enhanced (vide supra).

Finally, the RREP of complex 3 is similar to that of 2 and shown

in Figure S2.

Additional analysis^28-33of the RREP of the S pπ f Cu CT

band makes it is possible to obtain a quantitative estimate of

the magnitude of the excited-state distortion of the Cu-S bond

associated with this charge-transfer transition.^53,54Specifically

the dimensioned distortion along normal mode Q_n(∆Q_n, e.g., a

Cu-S stretch, with units of Å) is given by

5.805

∆Q_n)

‚ ∆

(1)

ν µ

x

n

where ∆ is a dimensionless normal-coordinate displacement

parameter, ν_nis the modal frequency (in cm^-1), and µ_nis the

(52) Spiro, T. G.; Czernuszewicz, R. S. Methods Enzymol. 1995, 246,

416-460.

(53) Gamelin, D. R.; Bominaar, E. L.; Mathonie`re, C.; Kirk, M. L.;

Wieghardt, K.; Girerd, J.-J.; Solomon, E. I. Inorg. Chem. 1996, 35, 4323-

4335.

(54) Henson, M. J.; Mukherjee, P.; Root, D. E.; Stack, T. D. P.; Solomon,

E. I. J. Am. Chem. Soc. 1999, 121, 10332-10345.

Cu(II)-Thiolate Complexes and Fungal Laccase

J. Am. Chem. Soc., Vol. 122, No. 47, 2000 11639

Table 3. Parameters for Fits of the S pπ f Cu CT Band in 2 (Γ

) 500 cm^-1

)

ν(i)/cm^-1

∆(i)

E_R(i)/cm^-1

930

% contrib

428

540

1300

370

2.08

0.05

1.00

83

0

1

2

185

17

total E_R1120

molecular reduced mass (in g/mol). The absolute magnitude of

the dimensionless normal-coordinate displacement parameter,

∆, is determined from a time-dependent^28-33simulation of the

absorption spectrum and the Raman enhancement profile using

a self-consistent set of parameters (Figure 5).

The parameters used to simulate successfully the experimental

data for 2 are summarized in the first two columns of Table 3.

For the S pπ f Cu CT band at 752 nm in 2, both the 370 and

428 cm^-1bands show enhancement with ∆ values of 1.0 and

2.1, respectively. In contrast, the π-π* band at 350 nm shows

strong enhancement of the 1300, 540, and 370 cm^-1vibrations

that have absolute ∆ values of 1.2, 1.4, and 1.0, respectively.

The excited-state vibrational relaxation energy, E_R, corresponds

to the total amount of vibrational energy of the individual modes

associated with the difference in electronic structure upon

changing from the ground state to the excited state, that is, E_R

) Σ_iE_R(i) ) Σ_i1/2 k_i(∆Q_i)². The vibrational relaxation energy

of the different modes (E_R(i)) can also be determined by relating

the ∆ values determined above to the Huang-Rhys parameter

Figure 6. XAS spectra of complexes 1 and 2. (A) S K-edge spectra.

(B) Cu L-edge spectra. Complex 1 - dotted line; Complex 2 - solid

line. Table 4 presents key spectral metrics.

S: S_i) E_R(i)/ν_i) ∆²/2.^46,53,55The second relationship gives

i

the relaxation energies for the S pπ f Cu CT band of 2 that

are included in Table 3. The total relaxation energy is much

smaller for 2 (1100 cm^-1) than for 1 (2600 cm^-1). As expected,

the largest contribution (85%) to this energy is associated with

the Cu-S stretching mode (Table 3).

Table 4. S K-edge and Cu L-edge XAS Data

S K-edge data:

compound

preedge

%S

energy (eV)^a

intensity^b

covalency^b

1

2

2469.0

2469.2

1.28

0.85

52 ( 1.2

32 ( 2.5

To approximate the vibrational system so that the excited

state distortion can be determined, we consider only the Cu-S

fragment and that the 428 cm^-1mode corresponds to a stretch

of this fragment. The strong relative intensity of this band in

the rR spectrum in Figure 3 suggests that this is a reasonable

approximation. Equation 1 can now be used to determine the

excited-state distortion. Within this approximation, the dimen-

sioned distortion along the normal coordinate (∆Q) directly

relates to the change in the Cu-S distance (i.e., ∆r ) ∆Q).

Since in the excited state, an electron occupies the S pπ

antibonding orbital at the expense of the bonding orbital, the

distortion will, in fact, be an elongation along this bond. Based

on this analysis, the Cu-S elongation in the S pπ f Cu CT

excited state of 2 is 0.12 Å, which is significantly smaller than

that for complex 1 (0.20 Å).²⁰This is largely due to the smaller

magnitude of the dimensionless normal-coordinate displacement

parameter, ∆, value for 2 (∆ ) 2.1) relative to 1 (∆ ) 3.3).

Since both complexes incorporate the same sterically hindered

triphenylmethylthiolate, the differences between the CT excited-

state distortions are due to the effects of differences in the Cu-N

interactions on the thiolate-Cu bond (vide infra).

Cu L-edge data:

compound

peak

intensities

%Cu

positions (eV)^a

covalency^b

L₂

930.8

931.3

L₃

950.8

951.3

L₂

4.07

3.68

L₃

1.04

0.97

1

2

36 ( 0.4

33 ( 0.8

^aEnergies reported are within an error of (0.1 eV. ^bError reported

is the standard deviation of all good fits, an additional 3-4% error is

introduced by the normalization procedure.

the S and Cu characters in the HOMO (Ψ_HOMO≈ [1 - R²]^1/2

|Cu 3d - R |S 3p ) can be directly probed by measuring the

intensities of the dipole allowed S 1s f HOMO or Cu 2p f

HOMO transitions, while the relative energies of the edge and

preedge features in the spectra give further insight into the

electronic structure.

3.4.1. Intensities. The S K-edge spectrum of complex 2 is

compared to that of complex 1 in Figure 6A. Using plastocyanin

as a reference with 38% S 3p character in the HOMO,⁵⁸the

intensity of the preedge feature in the S K-edge XAS spectrum

of 2 gives 32% S 3p character in the HOMO (Table 4). In

contrast, the HOMO of complex 1 shows 52% S p character.²⁰

Thus, in 2 there is substantially less S p character in its HOMO,

even though this complex utilizes the same triphenylmethyl-

thiolate ligand as 1. This difference in thiolate S character in

the HOMO reflects the effect of the difference in the nitrogen

ligation for the two systems. Finally, the reduced S 3p character

3.4. Metal and Ligand XAS Spectroscopy. XAS experi-

ments at the S K- and Cu L-edges can provide quantitative

information about the electronic structure of a complex including

details of the HOMO wave function character.^56,57Specifically,

(55) Huang, K.; Rhys, A. Proc. R. Soc., London A 1951, 208, 352.

(56) Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc.

1990, 112, 1643-1645.

(57) Glaser, T.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. Acc. Chem.

Res. 2000. In press.

(58) Shadle, S. E.; Penner-Hahn, J. E.; Schugar, H. J.; Hedman, B.;

Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1993, 115, 767-776.

11640 J. Am. Chem. Soc., Vol. 122, No. 47, 2000

Randall et al.

in the HOMO of 2 relative to 1 is consistent with the

substantially reduced oscillator strength in the absorption

spectrum noted previously.

Scheme 1

The Cu L-edge XAS spectra of complexes 1 and 2 are

compared in Figure 6B. Using D_4h[CuCl₄]^2-as a reference

complex with 61% Cu character in its HOMO,⁵⁹the HOMO of

2 has 33% Cu character (Table 4). This is slightly less than the

36% Cu character observed for 1. Although the combined S

and Cu covalencies determined with this XAS analysis imply a

covalent thiolate interaction in 2, they account for only ∼65%

of the total wave function character. This suggests that there is

another significant covalent interaction in the HOMO of 2. The

large ¹⁴N superhyperfine coupling observed in its EPR spec-

trum¹⁹implies that this covalency is contributed by N character

in the HOMO of 2 (vide infra). In addition, Cl K- and Cu L-edge

XAS of the chloride analogues of 1 and 2 indicates similar Cl

covalency in both complexes, but increased Cu character in the

Cl analogue of 1 (73% Cu character) relative to the Cl analogue

of 2 (48% Cu character) (see Supporting Information, Figure

S3), further supporting the significant contribution from the

â-diketiminate ligand in the ground-state wave function of 2.

3.4.2. Edge and Preedge Energies. The energies of the S

K-edge feature |S 1s f |S 4p for 1 and 2 both exhibit a first

derivative inflection point at 2471.5 eV. This indicates that the

sulfur 1s core orbitals lie at similar energies in these two

complexes and therefore that the effective nuclear charges of

the thiolate sulfurs in these two compounds are virtually

identical. This implies that the S(thiolate) atoms in both

complexes are similar donor ligands, which is consistent with

the similarities of the Raman Cu-S stretching frequencies

observed for the two complexes. The sulfur preedge feature in

2 occurs at 2469.2 eV (Table 4) and is 0.2 eV higher than the

preedge feature in complex 1. Because the edge energies of these

two compounds are so close, the preedge energy difference

represents the combined effects of shifts in the entire d-orbital

manifold due to changes in the Z_effof Cu and differences in the

ligand field splitting (vide infra).

the same energy in 1 and 2. Further, the MCD results (Figure

2B) make it clear that the ligand field of 2 is larger than in 1,

with the average energy of the “initial state” d f d transitions

in 2 being 6800 cm^-1(∼0.8 eV) higher than in 1.²⁰Including

this information for these three cases, the pattern of S K- and

Cu-L preedge transition energy shifts for complex 2 relative

2-1

to 1, ∆_S-K

and ∆_Cu-L^2-1, in Scheme 1 can be predicted.

Application of this analysis to the observed XAS data will enable

us to evaluate the Z_effof Cu in 2 relative to that in 1.

If the Z_effof Cu in 1 and 2 were equal, case (i), ligand field

effects alone, which are observed with optical spectroscopy (vide

supra), would dominate the shifts of the preedge features in

XAS spectra. This suggests that both the S K- and Cu-L-

preedges for 2 should be at higher energy than for 1 by a similar

amount that would correspond to the “final state” (|d¹⁰c )⁶¹

2-1

ligand field difference of the two complexes (i.e., ∆_Cu-L

≈

∆

S-K

^2-1). The magnitude of the experimentally observed shifts

in the S K- and Cu L-preedge features are not equivalent (0.2

eV for S K-edge and 0.5 eV for Cu L-edge); thus, this case

does not apply. In case (ii), the decreased Z_effof 2 relative to 1

would shift both the core Cu 2p orbitals and the valence orbitals

to less deep binding energy, but the magnitude of the effect on

the core orbitals should be greater. This suggests that the Cu

L-edge transition of 1 would be at higher energy than for 2.

Further, the decreased Z_effof 2 relative to 1 would combine

with the larger ligand field of 2 to give a large S K-preedge

transition energy difference. In addition to the incorrect predic-

tion of the relative Cu L-preedge energies of 2 and 1, the

The Cu L-edge XAS spectra presented in Figure 6B show

that both the L₃(∼931 eV) and L₂(∼951 eV) edges are about

0.5 eV higher in 2 than in 1 (Table 4). The energies of the Cu

L-edge transitions (Cu 2p f 3d, HOMO) depend on the metal

ligand field, the overall energy of the d manifold, and shifts in

the Cu 2p core energy level (vide infra).⁶⁰

3.4.3. XAS Comparison of 1 to 2. Contained in XAS preedge

energies is information about the relative effective nuclear

charge (Z_eff) of the copper atom in complexes 1 and 2. However,

the preedge energy has contributions from the ligand field

splitting, the energy of the entire d-manifold, which is affected

by Z_eff, and the core level energies. A more positive Z_efffor Cu

will shift the entire d-manifold to deeper binding energy.⁶⁰By

examining the relative preedge and edge energies in 1 versus 2

at the Cu L- and S K-edge regions, we can determine the relative

Z_effvalues for the two complexes. Scheme 1 summarizes the

three possibilities for the relative Z_effof Cu in the two

complexes: (i) if Z_effin 1 were equal to Z_effin 2, their

d-manifolds would be at identical energies; (ii) if Z_effin 1 were

more positive than in 2, the d-manifold of the latter would be

to less deep binding energy; (iii) if Z_effin 1 were less positive

than in 2, the d-manifold of the latter would be at deeper binding

energy. Based on the similar edge energies in the S K-edge

data for the two complexes, the S(thiolate) 1s core levels are at

2-1

predicted S K-preedge and Cu L-preedge differences (∆_Cu-L

and ∆_S-K^2-1) for this case are reversed from what is observed

experimentally. It is therefore clear that Z_effof 1 is not greater

than or equal to Z_effof 2. Finally, in case (iii), for the S

K-preedge energy, the increased ligand field of 2 would be offset

by its higher Z_effrelative to that of 1. These two effects would

largely cancel, leading to a small S K-preedge energy difference

between 1 and 2. At the Cu L-edge, the increased relative Z_eff

of 2 would shift both the core and valence orbitals to deeper

binding energy, though again the magnitude of the shift in the

core Cu 2p orbitals would be expected to be larger. Therefore

the Cu L-preedge transition energy of 2 would be expected to

be at higher energy than the transition of 1. Only case (iii)

predicts an energy shift pattern for both the Cu L-edge and S

K-edge data that is consistent with experiment. This clearly

demonstrates that the Z_effof the copper atom in 1 is less positive

than that of the Cu in 2 and further implies that the d-manifold

(59) George, S. J.; Lowery, M. D.; Solomon, E. I.; Cramer, S. P. J. Am.

Chem. Soc. 1993, 115, 2968-2969.

(60) Shadle, S. E.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. Inorg.

Chem. 1994, 33, 4235-4244.

(61) This represents the metal valence configuration after formation of

core hole denoted by c.

Cu(II)-Thiolate Complexes and Fungal Laccase

J. Am. Chem. Soc., Vol. 122, No. 47, 2000 11641

The isotropic portion of the observed nitrogen superhyperfine

interaction results from Fermi contact with the N 2s character

that is mixed into the σ-bonding ligand MO by hybridization,

while the anisotropic portion results from spin dipolar coupling

between the ¹⁴N nuclear spin and the unpaired (anisotropically

distributed) electron character in the N pz orbital that lies along

the Cu-N bond.^65,66The noncovalent electron-nuclear dipolar

coupling is a small fraction (5%) of these parameters; it is not

included in this analysis because it is on the order of the

uncertainty of the simulated values. Ligand field theory expres-

sions for the superhyperfine parameters A_|(¹⁴N) and A (¹⁴N)

can be written as:⁶⁵

¹⁴N

1

2

A_|(¹⁴N) ) â²‚ {n²A_Iso+ (1 - n²)A_Aniso

}

(2a)

( )

¹⁴N

1

( )

2

A (¹⁴N) ) â²‚ {n²A_Iso- ¹/₂(1 - n²)A_Aniso

}

(2b)

Here â²is the total nitrogen covalency (i.e., HOMO nitrogen

wave function character) and n²represents the degree of s

Figure 7. EPR spectrum of 2 and a simulation with the nitrogen

superhyperfine interactions aligned with their z′ directions along the

Cu-N bonds. Parameters are summarized in the text. Experimental

spectrum from ref 19.

hybridization of the â-diketiminate ligand orbital (i.e., Ψ_N,b1

≈

¹⁴N

[1 - n²] |N 2pz + n|N 2s ). The quantities A_iso

and

x

¹⁴N

A_Aniso

are calculated isotropic and anisotropic hyperfine

of complex 2 lies to deeper energy than in complex 1. In

summary, this analysis of the relative XAS preedge energies

indicates that the effective nuclear charge on the Cu is higher

in the three [2N + S] coordinate 2 than in the four [3N + S]

coordinate 1. These results clearly indicate that, while the

â-diketiminate is a strong in-plane donor ligand that leads to

reduced S pπ character in the HOMO, the additional ligand in

the axial position of the tris(pyrazolyl)hydroborate ligand

provides a stronger net donor interaction with the Cu.

couplings of one unpaired electron residing in the respective

¹⁴N

nitrogen orbitals (2s and 2pz) and are tabulated^65,67(A_iso

≈

¹⁴N

520 × 10^-4cm^-1and A_Aniso≈ 31 × 10^-4cm^-1). The factor

of ¹/₂outside of the braces corrects for the two symmetry-related

nitrogens in the HOMO. The parameters â²and n²in eqs 2 are

both unknown. However, solving eqs 2 simultaneously using

the experimentally determined superhyperfine values of A_|′ and

A ′ gives â²) 0.2-0.3 and n²) 0.1-0.2. In addition to

showing moderate s hybridization, this analysis demonstrates

that the HOMO of 2 has significant (∼25% N) nitrogen

covalency. This substantial N covalency accounts for the

majority of the HOMO wave function character that was

outstanding from the S K-edge and Cu L-edge XAS experiments

(vide supra). The small remaining wave function character

(∼10%) apparently resides on nonligating atoms including those

in the â-diketiminate ligand as well as the triphenylmethyl

group.

3.5. Analysis of Nitrogen Superhyperfine Coupling in the

EPR Spectrum. The EPR spectrum of 2 reveals a strong

nitrogen superhyperfine interaction in the g region,¹⁹as shown

in Figure 7. In contrast, no ¹⁴N superhyperfine coupling is

resolved in the EPR spectra of either fungal laccase or 1.^15,23,62,63

This suggests that there is considerable nitrogen character in

the HOMO of 2. For the ligating N atoms to exhibit considerable

covalency, the HOMO must be oriented in the trigonal N₂S

plane. Using simulations of the EPR spectrum that include this

superhyperfine interaction, the degree of N covalency can be

quantitated. To obtain this molecular information, it is necessary

to simulate the EPR spectrum with the ¹⁴N hyperfine interaction

matrix (‘tensor’) aligned with its z direction (z′) along the Cu-N

bond. This axis system is different than the molecular axis

system employed in the earlier EPR simulations where z is

perpendicular to the HOMO plane. Thus, the superhyperfine

interaction matrix must be rotated into this molecular axis system

in the spectral simulations. The spin Hamiltonian parameters

used in the slightly revised EPR simulation shown in Figure 7

are: g_x) 2.037, g_y) 2.037, g_z) 2.169, A_x(Cu) ) 4.7 × 10^-4

cm^-1(14 MHz), A_y(Cu) ) 9.3 × 10^-4cm^-1(28 MHz), A_z(Cu)

) 106.7 × 10^-4cm^-1(320 MHz), A_x′(N) ) 10 × 10^-4cm^-1

(30 MHz), A_y′(N) ) 10 × 10^-4cm^-1(30 MHz), A_z′(N) ) 14

× 10^-4cm^-1(42 MHz), where the two I ) 1 ¹⁴N atoms differ

only in their Euler angles and the prime on the nitrogen HF

parameters indicate that the directions are in the ligand axis

system (i.e., Cu-N direction ) z′); here the molecular (g and

Cu hyperfine) axis system places z perpendicular to the N₂S

plane.⁶⁴

The magnitude of the nitrogen superhyperfine and the degree

of covalency that it indicates attest to considerably larger

ground-state nitrogen covalency for 2 than for either complex

1 or for blue Cu centers such as fungal laccase or plastocyanin,

where no nitrogen superhyperfine is observed in the EPR

spectrum. Higher resolution EPR-derived spectroscopic tech-

niques have not been applied to 1, and it is not possible to make

a quantitative comparison between the model complexes.

However, based on ENDOR studies of several blue Cu sites,

Hoffman et al. have estimated a much lower N-ligand covalency

of ∼5% N per ligand.⁶⁸The large N covalency in the HOMO

of 2 is consistent with its reduced S p covalency observed with

XAS (vide supra).

(64) The EPR parameters in the text were simulated using first-order

perturbation theory. (Neese, F.; Zumft, W. G.; Antholine, W. E.; Kroneck,

P. M. H. J. Am. Chem. Soc. 1996, 118, 8692-8699.) Matrix diagonalization

approaches with QPOWA²⁶gives a slightly (∼4%) larger value for A_z(Cu)

of 111 × 10^-4cm^-1(332 MHz).

(65) Goodman, B. A.; Raynor, J. B. AdV. Inorg. Chem. Radiochem. 1970,

13, 135-362.

(66) McGarvey, B. R. In ESR and NMR of Paramagnetic Species in

Biological and Related Systems; Bertini, I., Drago, R. S., Eds.; D. Reidel:

Dordrecht, Holland, 1980; pp 171-200.

(62) Kitajima, N. AdV. Inorg. Chem. 1992, 39, 1-77.

(63) Penfield, K. W.; Gay, R. R.; Himmelwright, R. S.; Eickman, N.

C.; Norris, V. A.; Freeman, H. C.; Solomon, E. I. J. Am. Chem. Soc. 1981,

103, 4382-4388.

(67) Herman, F.; Skillman, S. Atomic Structure Calculations; Prentice

Hall: Englewood Cliffs, NJ, 1963.

(68) Werst, M. M.; Davoust, C. E.; Hoffman, B. M. J. Am. Chem. Soc.

1991, 113, 1533-1538.

11642 J. Am. Chem. Soc., Vol. 122, No. 47, 2000

Randall et al.

Figure 8. Calculated energy level diagram and orbital representations

for the high-lying valence orbitals of the â-diketiminate ligand. Key

orbitals are described in the text.

3.6. Density Functional Calculations. The experimentally

derived spectral features that have been described above for 2

relative to 1 include the following: the d f d transitions are at

higher energy; the S pπ f Cu CT transition is at lower energy

and of lower intensity; the Cu-S bonds exhibit similar strength;

the excited-state distortion, ∆_ES, is significantly reduced; the

HOMO has similar Cu character, reduced S(thiolate) character,

and enhanced N character; and the Cu Z_effvalue is more positive.

These data can now be used to evaluate electronic structure

calculations which can give further insight into bonding. First,

the â-diketiminate ligand system is defined. Subsequently, the

electronic structure of the Cu(II)-thiolate complex of this ligand

2 is evaluated and compared to complex 1.

3.6.1. Valence Orbitals of the Ligands.

3.6.1.1. â-Diketiminate Valence Orbitals. The electronic

structure of the planar, conjugated â-diketiminate ligand core,

which is modeled as C₃N₂H₅, is an important aspect of the

electronic structure of Cu complex 2 and permits an evaluation

of the equatorial ligand interaction. Note that the phenyl rings

that are appended to the nitrogens of this ligand are perpen-

dicular to the C₃N₂Cu plane¹⁹and are not part of the conjugated

π-system. Figure 8 shows an energy level diagram determined

by ADF calculations with schematic representations of the

highest energy â-diketiminate orbitals that might be involved

in bonding interactions with Cu. In this anionic ligand, the two

highest-lying orbitals are close in energy (∆E < 0.2 eV). The

HOMO (2b1) is characterized by out-of-plane p-type orbitals

on the two nitrogens and the central carbon (C3). In contrast,

the 5b2 orbital is characterized by in-plane, out-of-phase orbitals

localized on the nitrogens with lobes that point directly toward

the metal (Figure 8). In 5b2, the wave function character is

calculated to be mostly (39% N_calcper N) in the hybridized N

orbitals which would interact with the coordinated Cu. In

contrast, in the 2b1 orbital the wave function character is

Figure 9. Calculated energy level diagram and orbital representations

for the occupied, high-lying valence orbitals of complex 2 (â-

diketiminate trimethylthiolate Cu(II)). The â-diketiminate-localized

LUMO is also included. See Table 5 for a summary of the calculated

wave function characters.

π-antibonding analogy of 1a2. The HOMO-LUMO gap of the

ligand used (including the phenyl ligands) is 2.3 eV.

3.6.1.2. Thiolate. The thiolate orbitals were discussed fully

in the preceding paper.²⁰Briefly, the two important valence

orbitals that can interact strongly with the Cu d orbitals are

designated S pπ and S p pseudo-σ. These are the p orbitals on

the sulfur that do not interact with the alkyl carbon. The Cu-

S-C angle splits the energy of these orbitals. Further, the Spπ

distributed among the out-of-plane orbitals on C3 (37% C_calc

)

and the terminal Ns (28% N_calcper N). To deeper energy lies

the 6a1 orbital, an in-plane, in-phase analogue of 5b2 that could

also take part in ligand-metal bonding, though it would be

expected to be weaker since the energy denominator would be

larger. To still deeper binding energy lie the out-of-plane 1a2

and 1b1 orbitals that are unlikely to have significant interactions

with the metal orbitals. Between these last two orbitals lie the

highest phenyl ring derived orbitals (not shown). The LUMO

of the â-diketiminate ligand (2a2) is also important in the

spectroscopy of the complex (e.g., the ligand π f π* transition

at 350 nm, vide supra). The LUMO is characterized as the

2

orbital can undergo a π-symmetry interaction with the d_{x -y}

orbital, while the S p pseudo-σ orbital is oriented perpendicular

to the C-S bond and the S pπ orbital.

3.6.2. Description of Bonding in 2 and Comparison to

Spectra. An energy diagram of complex 2, as calculated with

DFT including the generalized gradient approximation as

implemented in the ADF package,^38,39is shown in Figure 9

along with representations of the highest lying molecular

orbitals. The wave functions of these orbitals are summarized

in Table 5. Three key orbitals, the HOMO (10a′′), the Cu-S

Cu(II)-Thiolate Complexes and Fungal Laccase

J. Am. Chem. Soc., Vol. 122, No. 47, 2000 11643

Table 5. Results of ADF Calculations for the Highest Valence Orbitals in the [C₃H₅N₂CuSCH₃] Approximation to 2

molecular orbital labels

10 A′′

x²-y²

16A′

π_nb,b1

15A′

d_xy

9A′′

S pπ

14A′

d_z

8A′′

d_yz+xz

13A′

d_yz-xz

12A′

S ps. σ

7A′′

op π_a2

6A′′

Nσ

11A′′

LUMO

2

energy (eV):

orb. contrib.

Cu d_z

-4.403

-4.875

-5.483

-5.933

-6.459

-6.563

-6.695

-7.311

-8.123

-8.491

-1.907

2

0

0.1

0

32

1

0.2

2

6

0

10

3

5

1

40

36

3

2

10

0

17

9

54

4

7

0

3

17

0.7

67

0

85

5

0.2

0.4

7

0

38

0

5

33

3

6

12

40

0

70

0.5

22

4

0

8

0

5

21

0.1

0.5

0.2

49

28

0

1.6

0

37

40

0.1

0.8

0.5

19

37

0

Cu d_yz

Cu d_xz

Cu d_xy

0.6

0

0.0

1.2

0.2

0.0

34

0

2

Cu d_{x -y}

11

17

6

46

4

20

6

1

0

Cu d total

Cu s+p total

S Total

77

0.1

1.5

0.1

8

74

0.7

7

5

0.9

10

40

2

CH₃Total

N Total

18^b

5

1.6

1.7

â-diket. Lig.^a

6

1.7

12

60

^aWave function character of the nonliganding atoms in the â-diketiminate ligand. ^bIn the HOMO there is 3.13% N 2s character and 15.23% N

2p character.

is supported by the positive shift in the EPR g-values from g_e

()2.0023), i.e., g_|> g > g_e. The calculations faithfully

reproduce the relatively small Cu character (32% Cu d_calc

)

obtained from the Cu L-edge measurements (33% Cu d).

Further, the significant thiolate covalency in the calculations is

consistent with the S covalency of the HOMO of 2 that was

measured with S K-edge XAS. Importantly, the calculations

reproduce the decreased thiolate character of 2 (40% S_calc

)

relative to 1 (49% S_calc), though not to the extent observed

experimentally with S K-edge XAS (32% S for 2 vs 52% S for

1). The reduction in the calculated thiolate character in the

HOMO of 2 is consistent with its reduced oscillator strength

relative to 1. Also, consistent with experimental observation,

the calculations reproduce the shift in HOMO wave function

character from the thiolate ligand to the N-ligand in 2 versus 1,

while the Cu character remains approximately constant. The

HOMO is also calculated to exhibit considerable (18% N_calc

)

nitrogen character which derives from an antibonding interaction

between the Cu orbitals and the 5b2 orbital of the â-diketiminate

ligand. The large N character calculated in the HOMO (18%

N

_calc) agrees reasonably well with the experimental covalency

(â²

) 0.2-0.3) and s-p hybridization (n²

) 0.1-0.2)

expt

derived above from the significant ¹⁴N hyperfine observed in

the EPR spectrum.^19,72Thus, the calculations quite reasonably

reproduce many key experimentally derived ground-state prop-

erties of 2, and reproduce ground state differences between 1

and 2.

3.6.2.2. Excited Electronic States. Spectral Patterns and

Assignments for 2. The calculated one-electron energies reflect

the experimental trends in the relative energies of the excited

states. To 0.5 eV deeper binding energy than the HOMO in

Figure 9 lies the nonbonding 2b1 â-diketiminate-based MO

(π_nb,b1or 16a′). Next, the calculations predict that the d_xyorbital

(15a′) has an antibonding interaction with the S p pseudo-σ

orbital. In the middle of the ligand field levels lies the S pπ

bonding orbital (9a′′). Due to significant ligand orbital-ligand

orbital overlap between MO 9a′′ (S pπ-Cu bonding, Figure 10B)

and the HOMO of 2 (Figure 10A) which relates to the absorption

Figure 10. Orbital contours for three important molecular orbitals of

2

complex 2: (A) Cu d_{x -y}HOMO (10a′′) showing the S pπ antibonding

and N σ antibonding interactions; (B) S pπ bonding orbital (9a′′)

showing its N σ antibonding interaction; and (C) N-Cu bonding orbital

(6a′′).

pπ bonding orbital (9a′′), and the Cu-Nσ bonding orbital (6a′′),

are detailed in the contours in Figure 10.

3.6.2.1. HOMO. The redox-active, half-occupied HOMO

(69) Penfield, K. W.; Gewirth, A. A.; Solomon, E. I. J. Am. Chem. Soc.

1985, 107, 4519-4529.

shows the now familiar^{11,21,22,69-71}π-type antibonding interac-

(70) Larsson, S.; Broo, A.; Sjo¨lin, L. J. Phys. Chem. 1995, 99, 4860-

2

tion between the d_{x -y}and S pπ orbital (Figure 10A). This is

similar to the interaction present in the HOMO of 1 and many

blue Cu proteins. In analogy to 1 and blue Cu proteins, where

this interaction was first observed,^21,69the calculations indicate

that this interaction is very covalent with 32% Cu d_calcand 40%

4865.

(71) Pierloot, K.; Dekerpel, J. O. A.; Ryde, U.; Roos, B. O. J. Am. Chem.

Soc. 1997, 119, 218-226.

(72) Using the values of â²and n²calculated with DFT (Table 5), the

¹⁴N superhyperfine parameters can be calculated to be A_{|, calc}′ ≈ 12 × 10^-4

cm^-1and A _{, calc}′ ≈ 8 × 10^-4cm^-1in good agreement with the experimental

2

S

_calc(Table 5). The Cu d_{x -y}character calculated for the HOMO

values of 14 × 10^-4cm^-1and 10 × 10^-4cm^-1

.

11644 J. Am. Chem. Soc., Vol. 122, No. 47, 2000

Randall et al.

Table 6. Comparison of Total Cu 4s + 4p Contributions to Cu-S

π and σ Bonding and Antibonding Orbitals

intensity, it is clear that a transition from the 9a′′ orbital to the

HOMO (10a′′) yields the intense, low-energy S pπ CT transition.

Clustered, to deeper binding energy than the S pπ bonding

Cu orbital

HB(pz′)₃1^a

â-ket. 2^a

2

orbital are the d_z, d_yz-xz, and d_yz+xzorbitals. Below these orbitals

4s

4pz

4p σ

4p π

total p

total s + p

1.84

0.72

4.16

3.52

8.40

10.24

5.47

0.37

3.79

6.44

10.60

16.07

lie the S p pseudo-σ bonding orbital, the â-diketiminate-derived

1a2 orbital, which has a weak δ-type bonding interaction with

the Cu d_yz+xzorbital, and the N σ-bonding orbital. The spectral

pattern predicted by the calculations in which the S pπ f Cu

CT band is embedded in the LF bands is consistent with

experiment (Figure 2). However, the calculations reverse the

^aThe values are percent of an electron

2

observed order of the d_zand d_xyorbitals. The assignment from

also reproduce the substantial blue-shift of the ligand field

transitions in 2 relative to 1. A metric of this in 1 versus 2 is

the difference between the one-electron energies of the deepest

experiment (in Table 1) is consistent with the EPR-derived g

||

value, which provides an independent measure of the relative

d_xyf HOMO transition energy.⁷³Only assigning the higher

energy of these two d f d bands as d_xygives the correct

correlation between MCD and EPR spectral results over a series

of blue Cu proteins.¹⁵

2

d orbital (d_yz-xz) and the HOMO (d_{x -y}), (∆d-d_max). By this

measure, the calculated LF splitting in 2 is 10500 cm^-1larger

than in 1, in reasonable agreement with the experimental

difference of 8700 cm^-1. Thus, the calculations reproduce the

decrease in the energy of the S pπ f Cu CT transition and the

higher energy of the d f d bands observed in the MCD

spectrum effected by the stronger, trigonal ligand field in

complex 2 compared to complex 1.

3.6.3. Insights from the Calculations. The above points

clearly demonstrate that the ADF density functional electronic

structure calculations reproduce experimental trends reasonably

well. Therefore, we are now in a position to use the calculations

to gain further insight into the differences in the electronic

structures of 2 and 1.

Further, the calculations provide insight into the unassigned

bands 2, 7, and 8 observed in the absorption and MCD spectra

(Figure 2). Band 2 is likely due to a π_nb,b1f HOMO transition,

which is calculated at fairly low energy. However, the relative

ordering of π_nb,b1and the lowest-energy LF transition is reversed

in the calculations. Candidates for bands 7 and 8 in Figure 2

are two of the three deep-lying orbitals in Figure 9: S p pseudo-

σ, â-diketiminate π_a2, and Nσ. Since the HOMO exhibits

considerable N covalency the NσfHOMO absorption would

be expected to exhibit an intense absorption, which is not the

case for band 7 or 8. Further, Raman excitation into the Nσ f

HOMO CT transition should give substantial excited-state

distortion and therefore a large Raman enhancement. Figure 5

demonstrates that these bands show very little Raman enhance-

ment at any vibrational frequency, further arguing against their

assignment as Nσ. Based on their calculated energy positions

and similarities in MCD sign with analogous copper thiolate

systems where the pseudo-σ band is positive, we suggest that

band 7 is the S p pseudo-σ f HOMO transition and band 8

involves a â-diketiminate π_a2orbital whose MCD intensity

derives from the weak δ-type interaction. The Nσ f HOMO

transition likely lies among the bands to higher energy than 9.

Finally, the calculated LUMO for the complex is localized on

the â-diketiminate ligand and analogous to the out-of-plane π*

2a2 orbital in the free ligand (Figures 8 and 9). The high

frequency of the Raman vibrations (Figure 3B) that are

resonance enhanced in band 9 suggests that this band is

associated with a large excited-state distortion along C-C or

C-N bonds. Such a distortion would be expected for an

electronic transition from π_nb,b1to π_a2*, where the C-N π

interactions in the â-diketiminate ligand go from nonbonding

to antibonding, which supports the assignment for this band.

3.6.2.3. Excited-State Comparison to 1. These calculations

also reproduce the observed spectroscopic trends in compound

2 relative to compound 1. Specifically, in 2 the S pπ - Cu

bonding orbital is calculated to be embedded in the d orbital

block (Figure 9), while the calculations on 1 placed the thiolate

S pπ bonding orbital to deeper binding energy than the ligand

field block, consistent with experimental observation (Figure

2). In addition to the relative position of the CT transition, the

calculations also predict the experimental red-shift of the CT

transition: in 2 the difference between the one-electron orbital

energies of the HOMO and the S pπ bonding orbital is ∼2000

cm^-1less than the analogous difference in 1. The calculations

3.6.3.1. Strength of the Thiolate Bond. The calculations

reflect the decrease in S thiolate p character in the HOMO of 2

relative to 1 that was observed with the S K-edge experiments.

This results from strong interaction in the HOMO and the Cu

2

S pπ bonding orbital between the Cu d_{x -y}and the â-diketimi-

nate ligand orbital concomitant with a weaker thiolate S pπ -

2

Cu d_{x -y}interaction as seen in Figures 10A and 10B. Thus, in

2 there appears to be a trans influence in which the greater

donor strength of the â-diketiminate ligand reduces the strength

2

of the thiolate S pπ interaction with the Cu d_{x -y}orbital.

The reduced S pπ character in the HOMO derived from

experimental and computational results might appear to be

inconsistent with Raman data that suggests the total strength of

Cu-S bonds are similar in complexes 1 and 2, because the

thiolate S-Cu vibrational frequency is so similar for the two

complexes (421 cm^-1in 1 versus 428 cm^-1in 2). However,

the calculations (Table 6) indicate that there is more 4s and 4p

character in the S pπ and S pσ bonding and antibonding orbitals

2

of 2 (10a′′ ) d_{x -y}, 15a′ ) d_xy, 9a′′ ) S pπ, and 12a′ ) S

pseudo-σ) relative to the analogous orbitals in 1. The Cu 4pπ

(orbital lobes in the equatorial plane but perpendicular to the

Cu-S bond) and 4s interactions in 2, in particular, are

significantly larger than in 1. These MOs reflect enhanced S

bonding interactions in 2 with these Cu orbitals relative to 1,

which compensates for the reduced S pπ-type interaction. Thus,

while the S pπ character in the HOMO is different between the

two complexes, their net Cu-S bonding interactions are very

similar. The calculations suggest that this is due to thiolate-Cu

orbital interactions that were not reflected in the sulfur K-edge

intensity.

3.6.3.2 Behavior of the Low-Energy S pπ CT Transition.

On the basis of the experimental evidence presented above it is

clear that the 750 nm band in 2 is the S pπ f Cu CT transition.

The calculations support this assignment. While the oscillator

strength of this band is reduced relative to 1 (f_exp,sc(2) ) 0.066

vs f_exp,sc(1) ) 0.077, vide supra), in complex 2 this band still

exhibits significant intensity, reflecting a covalent Cu-S pπ

(73) Since the shift in the g_|value from g_e(∆g_|) g_|- g_e) is inversely

proportional to the d_xyfHOMO transition energy, assigning the lower energy

dfd band (band 1) as d_xywould predict a much greater ∆g_|than is

experimentally observed, see ref 15.

Cu(II)-Thiolate Complexes and Fungal Laccase

J. Am. Chem. Soc., Vol. 122, No. 47, 2000 11645

bonding interaction. In fact, the quantitative intensity (f_exp,sc

)

of the S pπ f Cu CT band in 2 (band 3) is higher than might

be expected considering the S K-edge XAS experiments that

indicate the S p character in the HOMO of 2 (32% S p) is

substantially reduced relative to 1 (52% S p). An additional

contribution to f_expin 2 not present in 1 is the â-diketiminate

ligand, which can also contribute to the intensity of this

transition. Figure 10, A and B, shows that in 2 there are strong

σ-type Cu-N antibonding interactions in both the S pπ - Cu

antibonding orbital (HOMO) (18% N_calc) and S pπ bonding

orbital (9a′′) (19% N_calc). In contrast, in 1 the Cu-N antibonding

interaction in the S pπ bonding orbital is much weaker as judged

by its reduced nitrogen character.⁷⁴Figure 10 indicates that in

2, the N character in both the S pπ bonding MO and the HOMO

involves σ-type antibonding interactions between the 5b2

2

derived â-diketiminate orbital and the Cu d_{x -y}. Since the

intensity of a CT band largely derives from overlap of the ligand

orbitals in the ground and excited state and there is substantial

2

overlap of the N-ligand orbitals in 2 in the S pπ - Cu d_{x -y}

bonding and antibonding (HOMO) orbitals, the N character will

contribute additional intensity to the S pπ f Cu CT transition.

Time domain analysis of the RREPs (vide supra) gives a

quantitative estimate for the S pπ f Cu CT excited-state

distortion for the Cu-S bond (∆_ES(r_Cu-S)) in 2 relative to 1

that is consistent with the above analysis of nitrogen-derived

intensity in the S pπ f Cu CT band in 2 but not 1: for 2

∆_ES(r_Cu-S) ≈ 0.12 Å in comparison to 1 where ∆_ES(r_Cu-S) ≈

0.20 Å.²⁰In 1, the large Cu-S distortion results from the strong

S pπ character in the HOMO. This interaction is substantially

reduced in 2, due to a trans influence resulting from the strong

â-diketiminate ligand contributions to the S pπ bonding orbital

and antibonding orbital (i.e., HOMO). The reduced Cu-S

character in these orbitals in 2 is consistent with its reduced

excited-state distortion, because the change in the Cu-S bonding

associated with the CT transition is smaller in 2 than in 1. There

is not a large distortion of the Cu-N bond since this interaction

is antibonding in both the donor and acceptor orbitals.

Figure 11. Calculated valence energy level diagrams showing

electronic structural changes upon converting from [HB(pz)₃]CuSMe

1 f [H₂B(pz)₂]CuSMe 4* f [H₅C₃N₂]CuSMe 2. The bold, horizontal

arrows on the right axis represent the average of the d-orbital energies,

E_LF. For complexes 1, 2, and 4* in order of decreasing binding energy

(i.e., increasing Cu Z_eff) these values are -5.47, -5.92, -6.59 eV,

sequentially.

Cu L- and S K- preedge features indicate that three-coordinate

complex 2 has a higher Z_effthan four-coordinate 1. This places

2

the d-orbital manifold (including the d_{x -y}HOMO) to deeper

binding energy which can contribute to a decrease in the S pπ

CT energy, though this could be partially offset by the increased

ligand field of 2 relative to 1.

3.6.4. Axial Ligand Effects. There are significant experi-

mental and theoretical differences between the electronic

structures of 1 and 2 (vide supra). It is possible to isolate the

origins of these differences (vide supra) by systematically

altering the geometry of 1 into 2. First the axial ligand is

removed to give 4*, a hypothetical trigonal bis(pyrazolyl)-

hydroborate ligated Cu thiolate. Next, the N-donor is changed

from pyrazole to â-diketiminate (i.e., complex 2). The effects

of these geometrical changes on the energies of the valence

orbitals are summarized in Figure 11.

Removing the axial ligand of 1 to generate the hypothetical

planar, three-coordinate complex 4* greatly increases the ligand

field splitting, which is rather small in 1 due to its more

tetrahedral geometry (∆dd_max) 8000 cm^-1in 1 vs 18400 cm^-1

in 4*). Further, in 4* the S pπ bonding orbital is calculated to

lie in the middle of the ligand field manifold. Both of these

trends are analogous to those observed experimentally when

comparing 1 to 2, demonstrating the importance of the axial

ligand. However, further electronic structural changes occur as

the equatorial nitrogen ligand is changed from two pyrazoles

in 4* to â-diketiminate in 2. Specifically, the one-electron energy

difference of the HOMO and Spπ bonding orbitals (an ap-

proximation to the S pπ f Cu CT transition energy) is

calculated to be ∼1000 cm^-1higher in energy in 4* than in 2.

This is partly due to a larger splitting of the Spπ bonding and

antibonding orbitals as reflected by increased S pπ character in

the HOMO of 4* (48% S_calc). It also results from destabilization

of the Spπ bonding orbital in 2 due to its substantial Cu-N

antibonding character.

Finally, the intense S pπ f Cu CT band in 2 (band 3) is

shifted to 2500 cm^-1lower energy than the analogous band in

1. In addition to the loss of the axial ligand, this reflects the

high donor strength of the â-diketiminate ligand. There are three

contributions to the reduced splitting between the S pπ bonding

and antibonding (i.e., HOMO) orbitals, which determines the

energy of the S pπ f Cu CT transition, in 2 relative to 1. First,

S K-edge XAS measurements suggest that there is substantially

less S p character in the HOMO of 2 (32% S) than in the HOMO

of 1 (52% S) due to the trans influence, which involves the

2

observed decrease in the S pπ interaction with d_{x -y}relative to

1. This reduces the splitting of the S pπ bonding-antibonding

pair, which reduces the energy of this CT transition. The second

factor relates to differences in the antibonding N character in

the S pπ bonding orbital (∼20% N_calcin 2 vs ∼12% N_calcin 1,

Figure 10B, but see footnote 74) This places the S pπ bonding

orbital to less deep binding energy than its counterpart in 1 and

contributes to a decreased S pπ CT transition energy in 2 relative

to 1. Finally, differences in the Z_effof Cu in 2 versus 1 due to

the loss of the axial ligand that are derived from observed XAS

edge shift patterns (vide supra) and calculations (vide infra),

influence this S pπ CT energy. The experimental shifts in the

(74) In complex 1 the N-ligand does interact with the S pπ bonding

orbital. However, this interaction involves N π orbital character that is

orthogonal to that in the HOMO. Therefore, there is little ligand-ligand

orbital overlap between the nitrogen contribution to the HOMO and Cu

Spπ bonding orbital in 1, and the N-ligand does not contribute to the

intensity of a CT transition between these donor and acceptor orbitals.

11646 J. Am. Chem. Soc., Vol. 122, No. 47, 2000

Randall et al.

Further, the HOMO of 4* is calculated to lie 0.85 eV to

deeper binding energy than the HOMO of 2. This HOMO shift

derives from a decreased effective nuclear charge in 2 relative

to 4* due to more efficient charge donation to the Cu from the

â-diketiminate ligand relative to the bidentate bis(pyrazolyl)-

hydroborate ligand. The horizontal arrows on the right ordinate

in Figure 11 show the average energy of the entire d-manifold.

These arrows indicate that in 4* relative to 1 the entire d-block

shifts to 0.85 eV deeper energy, which reflects a more positive

Z_efffor Cu in 4* due to the loss of the fourth (axial) ligand.

Maintaining the three-coordinate trigonal geometry, but chang-

ing the equatorial ligand from bis(pyrazolyl)hydroborate to

â-diketiminate, leads to an increase of the average d-block

energy that reflects the strong donor strength of the latter ligand

system relative to the former. However, the magnitude of the

influence of the (fourth) axial ligand on Z_effappears to be larger

than that of the equatorial ligand.

Thus, both axial and equatorial ligand effects modulate the

electronic structure of 1 versus 2. The absence of an axial ligand

in 4* and 2 increases the LF splitting. The red shift of the Spπ

CT band in 2 relative to 1 results from increases in Z_effcoupled

with strong â-diketiminate ligation that leads to reduced S pπ

bonding-antibonding splitting and a strong N-Cu antibonding

interaction in the S pπ bonding orbital. The nature of the

equatorial ligand is important because its donor strength can

modulate the strength of the Spπ interaction which in turn can

influence the magnitude of the S pπ bonding-antibonding

splitting, and therefore the energy of the S pπ f Cu CT

transition. In passing, we note that the calculations predict that

the HOMO of 2 lies 0.3 eV above that of 1 due to the opposing

influences from the relative ligand fields and the Z_effvalues of

the two compounds. This agrees reasonably well with the 0.2

eV shift to higher energy observed for the preedge feature in

the S K-edge XAS experiment. This shift in 2 results from the

partial cancellation of the stabilization of the d-manifold due

to the increased Z_eff, by the larger ligand field splitting of the d

orbitals of 2 relative to 1.

Scheme 2

features indicate that the effective nuclear charge of 2 is more

positive than for 1.

4.1. Nature of the â-Diketiminate: the trans Influence.

The â-diketiminate ligand in 2 imparts this three-coordinate,

trigonal complex with many of the unique aspects of its

electronic structure relative to four-coordinate, distorted tetra-

hedral complex 1. The negative charge of the â-diketiminate

ligand in 2 is localized on the planar [C₃N₂] unit. The resulting

destabilization of the orbitals of this anionic ligand is illustrated

by a high energy orbital, 5b2 (Figure 8), which has virtually all

of its wave function character on the nitrogen atoms. There is

a strong σ-type donation from this 5b2 ligand orbital into the

2

Cu d_{x -y}orbital, with which it has the appropriate phase to

interact. The strength of this interaction is reflected in the

substantial ¹⁴N superhyperfine observed in the EPR spectrum.

As depicted in Scheme 2, this leads to a trans influence where

the strong, in-plane interaction from the â-diketiminate ligand

2

donates considerable electron density to the Cu d_{x -y}at the

expense of the thiolate S pπ interaction with this orbital. This

trans influence is manifested in both the bonding and the

2

antibonding S pπ - Cu d_{x -y}combinations and leads to the

observed differences between the S pπ f Cu CT transition in

the absorption spectrum of 1 versus 2, including its lower

energy, lower oscillator strength, and smaller excited-state

distortion. Further, this trans influence leads to the diminished

S p covalency in the HOMO observed with S K-edge XAS.

4.2. Nature of the Cu-S Interaction. This trans influence

of the â-diketiminate ligand suggests that the thiolate bond

should be weaker in 2 than in 1. Raman spectroscopy, which

provides an experimental measure of the strength of the Cu-S

bond through the stretching frequency, indicates that this

expectation is not experimentally substantiated and that the

Cu-S bonds in the two compounds have rather similar overall

strengths, with 2 even slightly higher: ν(Cu-S) for 1 is 421

cm^-1, while ν(Cu-S) for 2 is 428 cm^-1. The similar S K-edge

energies from the XAS measurements confirm that the net donor

strength of S(thiolate) is similar in the two complexes. Calcula-

tions indicate that concomitant with the decrease in S pπ

character in the HOMO of 2 due to the trans influence, there is

a net increase in the Cu 4s and 4p mixing over the orbitals that

are involved in the S pπ and S p pseudo-σ bonding interactions.

These reflect donor interactions into the Cu 4s and 4p orbitals

that can compensate for the reduced S pπ character in the

HOMO and lead to comparable net Cu-S interactions. Thus,

the total Cu-S bonding is similar in 1 and 2, but the nature of

these bonding interactions is different.

4. Discussion

Although complexes 1 and 2 use the same strongly bonding

triphenylmethylthiolate ligand, the loss of the axial ligand in 2

relative to 1 and differences in the bonding with the nitrogen

ligands, tris(pyrazolyl)hydroborate in 1 and â-diketiminate in

2, impart these two complexes with differences in their

electronic structures. Geometrically, 2 is approximately trigonal

planar,¹⁹while 1 is approximately trigonally distorted tetrahe-

dral.^20,25,62This geometric difference manifests itself by present-

ing the Cu(II) ion with different ligand fields that can be probed

with MCD spectroscopy. The d f d bands in 2 are to

significantly higher energy (>8000 cm^-1) than in 1, which

suggests that the trigonal geometry, and the â-diketiminate

ligand associated with 2, provides a stronger ligand field than

in 1. Another manifestation of the electronic structural differ-

ences of these compounds is the altered spectral characteristics

of the S pπ f Cu CT transition of 2 relative to 1: it shifts to

lower energy, has reduced oscillator strength, and exhibits a

smaller Cu-S excited-state distortion. The intensities of the

XAS preedge features at the S K- and Cu L-edge regions point

to Cu-S covalency in 1 and 2, though there is less S p character

in the HOMO of 2 than 1. The ¹⁴N superhyperfine coupling

resolved in the EPR spectrum of 2 indicates that there is

significant nitrogen character in its HOMO, which partially

offsets the diminished S pπ interaction in this orbital. Further,

the relative energy pattern of the S K-edge and Cu L-edge XAS

4.3. Role of the Axial Ligand. The fact that the net donation

of the thiolate ligand in 2 is sufficient to give it a slightly

stronger Cu-S bond than in 1 (as revealed by the increase in

ν(Cu-S) from Raman) indicates the importance of the axial

ligand, or its absence, in tuning the electronic structure of these

molecules. For Cu thiolate systems without axial ligands, such

as 2 and fungal laccase, it has been proposed that the thiolate

Cu(II)-Thiolate Complexes and Fungal Laccase

J. Am. Chem. Soc., Vol. 122, No. 47, 2000 11647

can partially charge compensate for the missing axial ligand,¹⁵

which leads to the stronger Cu-S interactions that are observed

for these systems. The absence of an axial ligand in 2 also

increases the importance of the equatorial nitrogen ligands,

strengthening the donor interaction of the â-diketiminate ligand

with Cu d_{x -y}. In this respect, the magnitude of the trans

influence in 2 is a direct consequence of its trigonal (i.e., no

axial ligand) geometry.

20450 cm^-1in 2 versus 15600 cm^-1in fungal laccase). This

reflects the donor strength of the â-diketiminate ligand relative

to the analogous bis-imidazole ligand set in fungal laccase.

Comparison of the EPR properties of 2 (g_|) 2.169, g )

2.037) to those of the blue Cu sites in fungal laccase (g_|)

2.201, g ) 2.045)¹⁵gives additional information about the

relative strengths of the ligand fields of these two compounds.

2

The ligand field expressions (eqs 3) relate the shifts in g and

||

g from the free electron value, g_e) 2.0023, (∆g_q) g_q- g_e,

q ) |, ) to the energies of the ligand field transitions:

The edge and preedge energies in the S and Cu XAS

experiments indicate a more positive Z_efffor 2 than 1. Thus, in

three-coordinate complex 2 the d-orbital manifold is stabilized

relative to four-coordinate 1. This demonstrates that the axial

ligand plays a role in modulating Z_effthrough its additional donor

interaction with the Cu. Calculations confirm this, whereupon

removing the axial ligand of four coordinate [HB(pz)₃]CuSR₃

1 to give hypothetical three coordinate [H₂B(pz)₂]CuSR₃, 4*,

the d-manifold moves to substantially deeper binding energy

(arrows in Figure 11). Consistent with the XAS experimental

results, the calculations on 1 and 2 give a similar trend though

they involve different N-ligands (arrows in Figure 11). Relative

to complex 2, these theoretical results further indicate that

hypothetical complex 4* has a higher Z_eff, which confirms that

the â-diketiminate ligand is a more strongly donating bidentate

ligand than two pyrazoles, consistent with a substantial trans

influence.

The axial ligand can also affect the overall ligand field. Our

previously reported data for the blue Cu center in fungal

laccase¹⁵and the calculations in Figure 11 indicate that the

absence of an axial ligand leads to an increase in the energy of

the d-d bands. This effect has been attributed to stronger in-

plane ligand donor interactions. In trigonal planar complex 2,

this same effect appears to be operative and, along with strong

N-donor interactions, is responsible for driving the ligand field

transitions to exceedingly high energy.⁷⁵

∆g_|(2) ) ∆g_|(laccase)E_xy(laccase)/E_xy(2)

(3a)

∆g (2) ) ∆g (laccase)E_xz,yz(laccase)/E_xz,yz(2) (3b)

Here E_Xrepresents experimentally determined dfd transition

energies, where the average of the d_yz+xzand d_yz-xzenergies are

used for E_xz,yz. These equations give the values of 2.177 and

2.035 for g and g , respectively, which are in good agreement

||

with the experimental values of 2. Further, this analysis

accurately predicts the decrease in ∆g of 0.03 (≈ 2.20-2.17)

||

for 2 relative to fungal laccase. This analysis demonstrates that

the ligand field changes between fungal laccase and 2 are

responsible for the changes in the g values. Likewise, the ^63,65Cu

metal hyperfine interaction (A_|), which is larger for 2 than for

fungal laccase (-107 × 10^-4cm^-1vs -92 × 10^-4cm^-1), is

scaled by the change in ligand field, as manifest in the relative

∆g and ∆g_|values. Applying the ligand field relation: A_|(2)

≈ 396 × 10^-4cm^-1[[∆g_|(2) - ∆g_|(laccase)] +³/₇[∆g (2) -

∆g (laccase)]] + A_|(laccase), gives an estimated A_|(2) of -106

× 10^-4cm^-1, in excellent agreement with experiment. Thus,

the ligand field effects induced by the absence of an axial ligand,

as discussed above, are also evident in the EPR spectral data.

Further, the S pπ f Cu CT transition in 2 shows reduced

transition energy and intensity relative to the analogous band

in fungal laccase at 600 nm. This energy shift of the CT band

in 2 results from the strong interaction with the â-diketimi-

nate ligand. Specifically, the combined influences of the reduced

S pπ interaction and the destabilizing antibonding nature of

the Cu-N interaction in the S pπ bonding orbital reduce the

splitting of the S pπ bonding-antibonding pair, which together

lead to the decreased CT energy. The band intensity can be

described using the oscillator strength, which for the CT band

in 2 (f_exp,sc(S pπ) is 0.066) is larger than in fungal laccase¹⁵

(f_exp(S pπ) 0.055). This implies greater total ligand character in

the HOMO of 2 relative to fungal laccase. However, this

intensity increase in the S pπ f Cu CT band in 2 is not due to

an increase in the thiolate covalency of 2 relative to fungal

laccase. In fact, S K-edge XAS, which directly measures the S

character in the HOMO, show less S character in 2 (32% S)

than in plastocyanin (38% S). This latter value represents a lower

limit for fungal laccase, since, based on the relative f_exp(S pπ)

values¹⁵and ENDOR results,⁶⁸the thiolate covalency in fungal

laccase appears to be larger than in the prototypical blue Cu

site in plastocyanin. These oscillator strength data can be

understood based on differences in mixing in the S pπ bonding

orbitals. In fungal laccase, this orbital is almost exclusively

Cu-S pπ in character. In 2, however, there is substantial (20%

4.4. Comparison to Fungal Laccase. Since 2 is a good

structural model complex for the blue Cu site in fungal laccase,

it is important to compare the spectroscopic features of these

two approximately trigonal Cu(II)-thiolate centers. The HOMO

in fungal laccase bears a similar overall appearance to the

HOMO of 2 in that they both exhibit a highly covalent

interaction between the Cu d_{x -y}and S pπ orbitals.¹⁵Yet, there

are significant differences in their respective electronic struc-

tures. First, EPR measurements¹⁹indicate that there is substan-

tially more nitrogen character in the HOMO of 2 than in fungal

laccase. This compensates for reduced S 3pπ character in the

HOMO of 2.

2

The results for both fungal laccase and complex 2 indicate

the importance of the axial ligand in modulating the strength

of the ligand field. Upon changing from the prototypical blue

Cu site in plastocyanin with an axial S(Met), to fungal laccase

where this ligand is replaced by nonligating Phe or Leu to give

a trigonal Cu(II) center, the ligand field is shifted to higher

energy. The effect is even more dramatic if tetrahedrally

distorted stellacyanin, with an axial O(Gln) ligand,¹³is used as

the reference state.¹¹A similar effect is observed in the model

complexes compared in this study: upon removing the axial

pyrazole ligand from 1, the ligand field in trigonal 2 dramatically

increases. Relative to fungal laccase, whose ligand field

transitions are at high energy among blue Cu centers,¹⁵the

ligand field transitions in 2 are at even higher energy (d_yz-xzat

N

_calc) Cu-N σ antibonding mixed into this level. The same

Cu-N interaction is present in the HOMO of 2 and can

contribute to the intensity of the low energy CT band since the

ligand-ligand overlap from the N ligand orbital will be

significant.

(75) From Figure 11, the loss of an axial ligand decreases the energy of

2

the d_zorbital as observed experimentally (in 1, the z f x - y transition

(band 1) is at 5200 cm^-1while in 2 it is at 6300 cm^-1). The calculated

change in energy is larger than that observed experimentally, which appears

Finally, the MCD C-term signs in 2 are as observed in fungal

2

to be due to an overestimate in the 4s/d_zmixing in 2.

laccase with the exception of the low-energy d_ztransition (at

11648 J. Am. Chem. Soc., Vol. 122, No. 47, 2000

Randall et al.

6300 cm^-1), where this band exhibits positive sign in 2 but was

negative in fungal laccase. The sign of an MCD band depends

on the degree of ground- and excited-state spin-orbit coupling

to different states.⁷⁶The magnitude of this coupling depends

for 1 and 2 demonstrate that the total copper-thiolate bonding

interactions in the two models are similar, which suggests

compensation for the trans influence of â-diketiminate in the

HOMO of 2 through thiolate bonding with Cu 4s and 4p orbitals.

Thus, the loss of an axial ligand can modulate the electronic

structure of blue Cu centers, through an increase in equatorial

ligand donation. An increase in the covalency of the thiolate-

Cu bond can affect the reorganization energy and increase

electronic coupling into protein pathways for rapid electron

transfer.

2

inversely on the energy splitting between the d_zstate and the

ligand field or charge-transfer state that spin-orbit couples to

it. Because, relative to fungal laccase, the ligand field states in

2 are at much higher energy, while the S pπ f Cu CT state is

at much lower energy, the degree of spin-orbit coupling

between these states will be very different. In plastocyanin the

2

sign of the d_zf HOMO transition is due to mixing of z

Acknowledgment. We thank Professor Thomas Brunold for

the MathCAD script used for the time domain Raman analysis,

Dr. Frank Neese for his EPR simulation program, as well as

Professor Lawrence Que, Jr. and Dr. Raymond Y. N. Ho for

access and assistance with resonance Raman spectroscopy at

Minnesota. Financial support for this research program came

from the NSF (CHE-9980546 to E.I.S.) and the NIH (GM-47365

to W.B.T.; RR-01209 to K.O.H.; GM-18812 to D.W.R.; GM-

18991 to P.L.H.). SSRL operations are funded by the U.S.

Department of Energy, Office of Basic Energy Sciences. The

Structural Molecular Biology program at SSRL is supported

by the National Institutes of Health, National Center for

Research Resources, Biomedical Technology Program and by

the Department of Energy, Office of Biological and Environ-

mental Research.

polarization intensity associated with the Cu being displaced

from the N₂S plane by ∼0.3 Å.^10,15In fungal laccase the Cu is

in this plane, and this mechanism for MCD intensity is

15

2

eliminated, leading to the change in sign of the d_ztransition.

In 2, the Cu is displaced from of this plane by ∼0.2 Å,¹⁹which

provides a spin-orbit mixing mechanism similar to plastocya-

nin. Thus, the observed out-of-plane shift of the Cu in 2 has

electronic structural consequences.

In summary, for the two Cu(II) thiolate systems compared

in this study, the absence of an axial ligand in 2 relative to 1

greatly contributes to the spectroscopic differences between the

model complexes. The σ-donating bidentate â-diketiminate

equatorial ligand in 2 also makes an important contribution to

its electronic structure. Along with the loss of the axial ligand,

these modifications contribute to the observed decrease in the

S pπ f Cu CT transition energy and the increase in the d f d

transition energies. Further, relative to 1, the stronger N-donor

ligand in 2 changes its HOMO, through the increase in N

covalency (as observed with EPR), and leads to a trans influence

that decreases the thiolate covalency in the HOMO (as observed

with S K-edge XAS). Although the â-diketiminate is a strong

equatorial ligand, four-coordinate [3N + S] 1 has a lower Z_eff

for Cu than three-coordinate [2N + S] 2. The Raman spectra

(76) Neese, F.; Solomon, E. I. Inorg. Chem. 1999, 38, 1847-1865.

Supporting Information Available: Table of Raman iso-

tope shifts; figures showing: the rR spectrum of a second aryl

thiolate complex [HB(pz′)₃]CuSC₆F₅, the RREP for 3, XAS

spectra for the chloride starting materials of 1 and 2, and input

files for the calculations (PDF). An X-ray crystallographic report

(CIF). This material is available free of charge via the Internet

at http://pubs.acs.org.

JA001592O

Article Doi

Spectroscopic and electronic structural studies of blue copper model complexes. 2. Comparison of three-and four-coordinate Cu(II)-thiolate complexes and fungal laccase

DOI: 10.1021/ja001592o

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Article abstract of DOI:10.1021/ja001592o

Full text of DOI:10.1021/ja001592o

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